This course is structured to provide essential education regarding the epidemiology, prevention, diagnosis, and treatment of healthcare-associated infections (HAIs). The course begins with background information on the pathogenesis of bacterial infections, transmission of infection in the healthcare setting, and the development of drug resistance. The primary sources of HAIs related to the environment, patient factors, and iatrogenic factors are also discussed. The core of the course is a comprehensive description of the most common and costly HAIs: catheter-related urinary tract infections, surgical site infections, ventilator-associated pneumonia, intravascular device-related infections, and Clostridium difficile infections. The overall incidences, related costs, risk factors, common pathogens, prevention, diagnosis, and treatment are presented for each of these infections, with the implications of drug-resistant infections also noted. An overview of the responsibilities of an infection control program in the healthcare setting is provided, with a discussion of surveillance, adherence to infection control guidelines, management of drug-resistant microorganisms, precautions and isolation techniques, preparedness for outbreaks and epidemics, and education targeted to both healthcare workers and patients and families.
This course is designed for healthcare professionals who would benefit from enhanced knowledge of healthcare-associated infections, including physicians, physician assistants, nurses, surgical technologists/assistants, and others involved with the care of patients in hospitals, long-term care facilities, or other healthcare institutions.
NetCE is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. NetCE is accredited as a provider of continuing nursing education by the American Nurses Credentialing Center's Commission on Accreditation. NetCE is approved to offer continuing education through the Florida Board of Nursing Home Administrators, Provider #50-2405. NetCE is approved by the California Nursing Home Administrator Program as a provider of continuing education. Provider number 1622. NetCE is accredited by the International Association for Continuing Education and Training (IACET). NetCE complies with the ANSI/IACET Standard, which is recognized internationally as a standard of excellence in instructional practices. As a result of this accreditation, NetCE is authorized to issue the IACET CEU. This program has been pre-approved by The Commission for Case Manager Certification to provide continuing education credit to CCM® board certified case managers. The course is approved for 15 CE contact hour(s). Activity code: H00018126. Approval Number: 150004047. To claim these CEs, log into your CE Center account at www.ccmcertification.org.
NetCE designates this enduring material for a maximum of 15 AMA PRA Category 1 Credit(s)™. Physicians should claim only the credit commensurate with the extent of their participation in the activity. NetCE designates this continuing education activity for 15 ANCC contact hour(s). NetCE designates this continuing education activity for 10 pharmacotherapeutic/pharmacology contact hour(s). NetCE designates this continuing education activity for 18 hours for Alabama nurses. Successful completion of this CME activity, which includes participation in the evaluation component, enables the participant to earn up to 15 MOC points in the American Board of Internal Medicine's (ABIM) Maintenance of Certification (MOC) program. Participants will earn MOC points equivalent to the amount of CME credits claimed for the activity. It is the CME activity provider's responsibility to submit participant completion information to ACCME for the purpose of granting ABIM MOC credit. Completion of this course constitutes permission to share the completion data with ACCME. This continuing education activity is approved for 15 CE credits by the Association of Surgical Technologists, Inc., for continuing education for the Certified Surgical Technologist, Certified Surgical First Assistant and Associate members. This recognition does not imply that AST approves or endorses any product or products that are included in the enduring materials. This home study course is approved by the Florida Board of Nursing Home Administrators for 5 credit hour(s). This course is approved by the California Nursing Home Administrator Program for 10 hour(s) of continuing education credit - NHAP#1622010-5404/P. California NHAs may only obtain a maximum of 10 hours per course. AACN Synergy CERP Category A. NetCE is authorized by IACET to offer 1.5 CEU(s) for this program.
In addition to states that accept ANCC, NetCE is approved as a provider of continuing education in nursing by: Alabama, Provider #ABNP0353, (valid through December 12, 2017); California, BRN Provider #CEP9784; California, LVN Provider #V10662; Florida, Provider #50-2405; Iowa, Provider #295; Kentucky, Provider #7-0054 through 12/31/2017.
This activity is designed to comply with the requirements of California Assembly Bill 1195, Cultural and Linguistic Competency.
The purpose of this course is to provide physicians, nurses, pharmacists, microbiologists, and other healthcare professionals with enhanced knowledge of healthcare-associated infections, particularly an understanding of evidence-based guidelines, in order to prevent the most serious and common healthcare-associated infections and utilize the appropriate treatment options.
Upon completion of this course, you should be able to:
- Describe the effect of healthcare-associated infections on mortality, morbidity, and cost of health care, including the importance of surveillance and prevention.
- Outline the pathogenesis of infection and the development of antimicrobial resistance.
- Identify the environmental, patient-related, and iatrogenic risk factors for healthcare- associated infection.
- Describe the impact of nonimplanted and implanted devices and procedures on healthcare-associated infection.
- List the most common types of healthcare-associated infections.
- Identify the most common pathogens and risk factors associated with catheter-related urinary tract infections, and outline the appropriate prevention measures, diagnosis, and treatment.
- List the most common pathogens and causes of surgical site infections, and outline the appropriate prevention measures, diagnosis, and treatment.
- Define the most common pathogens and risk factors associated with healthcare-associated pneumonia, and outline the appropriate prevention measures, diagnosis, and treatment.
- Outline the most common pathogens and risk factors associated with intravascular device-related bloodstream infections, and discuss the appropriate prevention measures, diagnosis, and treatment.
- Discuss the risk factors and prevention strategies for nosocomial Clostridium difficile infection.
- List important hand hygiene techniques and strategies to increase compliance.
- Outline interventions to control influenza transmission in the healthcare setting.
- Describe the appropriate use of precautions and isolation techniques.
- Define additional elements of an institution's infection control program, including the education of healthcare workers and patients with respect to healthcare-associated infections and the need to address challenges in educating non-English-proficient individuals.
- Discuss the need for hospital preparedness for potential outbreaks.
Lori L. Alexander, MTPW, ELS, MWC, is President of Editorial Rx, Inc., which provides medical writing and editing services on a wide variety of clinical topics and in a range of media. A medical writer and editor for more than 30 years, Ms. Alexander has written for both professional and lay audiences, with a focus on continuing education materials, medical meeting coverage, and educational resources for patients. She is the Editor Emeritus of the American Medical Writers Association (AMWA) Journal, the peer-review journal representing the largest association of medical communicators in the United States. Ms. Alexander earned a Master’s degree in technical and professional writing, with a concentration in medical writing, at Northeastern University, Boston. She has also earned certification as a life sciences editor and as a medical writer.
Contributing faculty, Lori L. Alexander, MTPW, ELS, MWC, has disclosed no relevant financial relationship with any product manufacturer or service provider mentioned.
John M. Leonard, MD
Jane C. Norman, RN, MSN, CNE, PhD
Chris Keegan, CST, MS
The division planners have disclosed no relevant financial relationship with any product manufacturer or service provider mentioned.
The purpose of NetCE is to provide challenging curricula to assist healthcare professionals to raise their levels of expertise while fulfilling their continuing education requirements, thereby improving the quality of healthcare.
Our contributing faculty members have taken care to ensure that the information and recommendations are accurate and compatible with the standards generally accepted at the time of publication. The publisher disclaims any liability, loss or damage incurred as a consequence, directly or indirectly, of the use and application of any of the contents. Participants are cautioned about the potential risk of using limited knowledge when integrating new techniques into practice.
It is the policy of NetCE not to accept commercial support. Furthermore, commercial interests are prohibited from distributing or providing access to this activity to learners.
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#98781: Healthcare-Associated Infections
This course is structured to provide essential education regarding the epidemiology, prevention, diagnosis, and treatment of healthcare-associated infections (HAIs). The course begins with background information on the pathogenesis of bacterial infections, transmission of infection in the healthcare setting, and the development of drug resistance. The primary sources of HAIs related to the environment, patient factors, and iatrogenic factors are also discussed. The core of the course is a comprehensive description of the most common and costly HAIs: catheter-related urinary tract infections, surgical site infections, hospital-acquired pneumonia, intravascular device-related bloodstream infections, and Clostridium difficile infections. The overall incidences, related costs, risk factors, common pathogens, prevention, diagnosis, and treatment are presented for each of these infections, with the implications of drug-resistant infections also noted. An overview of the responsibilities of an infection control program in the healthcare setting is provided, with a discussion of surveillance, adherence to infection control guidelines, management of drug-resistant micro-organisms, precautions and isolation techniques, preparedness for outbreaks and epidemics, and education targeted to both healthcare workers and patients and families. The course content is limited to infections in adults in acute care hospitals, although many measures for prevention are applicable in all settings for all patient populations.
HAI is one of the leading causes of death and increased morbidity for hospitalized patients, affecting an estimated 1.7 million inpatients each year . Historically, these infections have been known as nosocomial infections or hospital-acquired infections because they develop during hospitalization. As health care has increasingly expanded beyond hospitals into outpatient settings, nursing homes, long-term care facilities, and even home care settings, the more appropriate term has become healthcare-acquired or healthcare-associated infection. Many factors have contributed to an increase in HAIs. Advances in medical treatments have led to more patients with decreased immune function or chronic disease. The increase in the number of these patients, coupled with a shift in health care to the outpatient setting, yields a hospital population that is both more susceptible to infection and more vulnerable once infected. In addition, the increased use of invasive devices and procedures has contributed to higher rates of infection; more than 80% of HAIs are caused by four types of infection: catheter-related urinary tract infection, intravascular device-related bloodstream infection, surgical site infection, and ventilator-associated pneumonia . These HAIs, along with infections caused by C. difficile and drug-resistant micro-organisms (especially methicillin-resistant Staphylococcus aureus [MRSA]), have garnered the most attention and research because of their impact in terms of morbidity, mortality, economic costs, and potential for prevention.
HAIs develop in an estimated 5% to 10% of hospitalized patients [2,3]. The infections are the cause of an estimated 99,000 deaths and add billions of dollars in total direct medical costs annually [2,4]. The increased focus on healthcare quality over the past decade has highlighted the need to prevent HAIs as part of overall efforts to enhance patient safety as well as reduce costs, and national initiatives have been developed by healthcare quality agencies, advocacy organizations, healthcare regulating bodies, and policymakers (Table 1) [5,6,7,8,9,10,11,12,13].
EXAMPLES OF NATIONAL INITIATIVES TO REDUCE FREQUENCY OF HEALTHCARE-ASSOCIATED INFECTIONS
|Agency for Healthcare Research and Quality: Making Health Care Safer: A Critical Analysis of Patient Safety, 2001 (25 safety practices)||
|Institute of Medicine: Priority Areas for National Action: Transforming Health Care Quality, 2003 (20 priority areas)||Prevent nosocomial infections and implement surveillance programs|
|Institute for Healthcare Improvement: 5 Million Lives Campaign, 2006 (12 safety interventions)||
|Surgical Care Improvement Project (partnership of several organizations), 2006||Reduce postoperative complications, including surgical site infections|
|Centers for Medicaid and Medicare Services (effective October 1, 2008)||No reimbursement for hospital costs related to catheter-associated urinary tract infections, vascular catheter-associated infections, and mediastinitis after coronary artery bypass graft surgery|
|U.S. Department of Health and Human Services, 2009||National Action Plan to Prevent Healthcare-associated Infections (9 targets for elimination of HAIs)|
|U.S. Department of Health and Human Services, 2011||Partnership for Patients: Better Care, Lower Costs|
|National Quality Forum: Patient Safety, 2012 (3 broad goals)||Goal 2: Reduce the incidence of adverse healthcare-associated conditions|
|The Joint Commission, National Patient Safety Goals, 2013 (6 broad goals)||Prevent Infection: Follow the CDC guidelines for hand hygiene, and use proven guidelines to prevent bloodstream infections from central lines, to prevent infection after surgery, and to prevent catheter-related urinary tract infections|
The U.S. Department of Health and Human Services developed the National Action Plan to Prevent Healthcare-associated Infections, an initiative with a steering committee that represents a host of government health-related agencies. The plan includes 5-year goals for nine specific measures of improvement in HAI prevention . Phase I of the plan calls for reducing the rate of HAIs in acute care hospitals; the authors of the plan note that a combination of 10 strategies is needed to prevent HAIs :
Reduce inappropriate/unnecessary use of devices
Improve adherence to hand hygiene and barrier precautions
Implement and improve antimicrobial stewardship
Clinical Leaders, Executives, and Administrators
Demonstrate leadership support at the highest levels of the facility
Implement a culture of safety
Government, Advocates, Clinical Leaders, and Administrators
Enhance financial incentives and regulatory oversight
Implement system-based approaches/ protocols/checklists
Achieve better use of technology
Improve public reporting of credible data
Enhance traditional and nontraditional partnerships
Evidence-based guidelines are at the heart of strategies to prevent and control HAIs and drug-resistant infections and address a wide range of issues from architectural design of hospitals to hand hygiene (Table 2) [15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38]. Adherence to individual guidelines varies but, in general, is low. For example, hand hygiene is the most basic and single most important preventive measure, yet compliance rates among healthcare workers have averaged 30% to 50% [26,39,40,41,42]. Decreasing the number of HAIs will require research to better understand the reasons behind lack of compliance with guidelines and to develop education and interventions that target those reasons.
SAMPLE OF GUIDELINES RELATED TO PREVENTING AND MANAGING HEALTHCARE-ASSOCIATED INFECTIONS
|American College of Chest Physicians/American Association for Bronchology||Consensus statement: prevention of flexible bronchoscopy-associated infection (2005)|
|American Institute of Architects||Guidelines for Design and Construction of Health Care Facilities (2014)|
|American Thoracic Society/ Infectious Diseases Society of America||Management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia (2005)|
|Canadian Critical Care Trials Group/Canadian Critical Care Society||Prevention of ventilator-associated pneumonia (2004)|
|Centers for Disease Control and Prevention (CDC)||
|Infectious Diseases Society of America||
|Society for Healthcare Epidemiology of America||
|Society for Healthcare Epidemiology of America/Infectious Diseases Society of America||Clostridium difficile infection in adults (2010)|
|Society for Healthcare Epidemiology of America/Infectious Diseases Society of America/Joint Committee on the Prevention of Antimicrobial Resistance||Prevention of antimicrobial resistance in hospitals (1997)|
|Society for Healthcare Epidemiology of America/Infectious Diseases Society of America (published as supplement to Infection Control and Hospital Epidemiology, 2008)||Strategies to prevent central line-associated bloodstream infections, ventilator-associated pneumonia, catheter-associated urinary tract infections, surgical site infections in acute care hospitals, and transmission of methicillin-resistant S. aureus and C. difficile infections|
|World Health Organization (WHO)||Prevention of Hospital-Acquired Infections: A Practical Guide, 2nd ed. (2002)|
"Zero tolerance" of HAIs became a common catch-phrase as a call to improve prevention strategies and eliminate HAIs. Zero tolerance for HAIs is a worthy goal, but the complete elimination of all HAIs is not feasible, primarily because interventions address only exogenous sources of infection and do not address many other important factors, such as host response, patient case mixes, pathogen virulence, and lack of specificity in definitions and diagnostic criteria [43,44]. Furthermore, the literature has not supported the complete elimination of HAIs with enhanced compliance to prevention protocols. The results of the CDC's Study of Efficacy of Nosocomial Infection Control (SENIC) suggested that 6% of all HAIs could be prevented by minimal infection control efforts and 32% by "well organized and highly effective infection control programs" [45,46]. A later review of 30 studies suggested that an estimated 20% of HAIs are preventable . A 2011 study estimated that approximately 65% to 75% of central line-associated bloodstream infections and catheter-associated urinary tract infections were preventable using current evidence-based strategies; 55% of ventilator-associated pneumonia and surgical site infections were estimated to be preventable . Furthermore, complete elimination is not needed to reap substantial benefit. The U.S. Department of Health and Human Services estimates that a 40% decrease in preventable HAIs (compared with the 2010 rate) would result in 1.8 million fewer injuries and more than 60,000 lives saved over 3 years . A 70% decrease in the rate of HAIs would save an estimated $25 to $31.5 billion .
The results of studies evaluating strategies to prevent HAIs have shown a wide range in efficacy, particularly with respect to specific HAIs. For example, the effectiveness of strategies to prevent surgical site infections has not been consistent, with some studies showing significant improvement and other studies showing no substantial improvement [49,50,51]. Still, research has shown that strict adherence to prevention interventions has an effect; one study demonstrated a decrease of as much as 66% in the prevalence of intravascular device-related bloodstream infections with adherence to a combination of interventions [52,53,54,55,56]. Combinations of interventions, or "bundles," have been found to be the most effective for preventing HAIs, and the Institute of Healthcare Improvement (IHI) has developed how-to guides on implementing these bundles, which are available for download from the IHI website [57,58,59]. More research is needed to determine the direct impact of many guideline recommendations and the combinations of "best practices" that yield the lowest rates of individual HAIs.
Among the national initiatives to reduce the number of HAIs was a move by the Centers for Medicare and Medicaid Services (CMS) to suspend reimbursement of hospital costs related to HAIs it considers "reasonably preventable:" catheter-related urinary tract infection, central line-associated bloodstream infection, and some surgical site infections [9,10]. However, studies have shown that this policy has not been a contributor to any decrease in the rate of HAIs, and a survey indicated that adherence to only some prevention strategies has increased as a result of the policy [60,61]. The policy also has the potential to lead to increased unnecessary use of antimicrobials in an effort to prevent infections .
In contrast, educating healthcare personnel helps to reduce HAIs, with a systematic review showing a statistically significant decrease in infection rates after an educational intervention in 21 of 26 studies . Education is one of the key elements found to be necessary for a successful HAI prevention program. When such programs at 33 diverse hospitals were evaluated, the following were found to be essential for success :
Educate and re-educate
Foster change by first understanding resistance
Engage frontline staff by involving them in the program and enlisting champions
Commit to regular strategic communication and join a collaborative
Start small and tailor implementation to local needs and cultures
Convince administration to provide leadership, funds, and dedicated staff and assign accountability
Provide timely, relevant feedback and celebrate successes
Accurate data collection is crucial for understanding trends and the burden of HAIs and for identifying emerging infectious threats. The Association for Professionals in Infection Control and Epidemiology (APIC), the Infectious Diseases Society of America (IDSA), and the Society for Healthcare Epidemiology of America (SHEA) have led efforts to establish uniform standards for surveillance of HAIs and standardized systems for collecting and reporting. The National Nosocomial Infections Surveillance (NNIS) system, managed by the CDC's Division of Healthcare Quality, was established in 1970 to monitor the incidence of HAIs, the responsible pathogens, and the associated risk factors. The NNIS can be used as a tool to assess risk and protective factors, evaluate preventive interventions, and provide information to event reporters and stakeholders. The National Health Safety Network (NHSN) was created to supersede the NNIS (as well as two other legacy CDC surveillance systems, the Dialysis Surveillance Network and the National Surveillance System for Healthcare Workers) . The NHSN includes voluntarily reported data on other healthcare safety events in addition to HAIs and provides standard definitions, protocols, and methodology. Reporting to NHSN is voluntary, and more than 17,000 medical facilities participate in the network .
In response to a call for mandatory reporting of HAIs, several states passed legislation requiring the mandatory reporting of specific HAIs, and reporting requirements vary by state. The number of states with mandates for public reporting grew from three in 2004 to 31 (and the District of Columbia) in 2015 [67,68].
A comprehensive description of the pathogenesis of infection is beyond the scope of this course. However, a broad overview of pathogen-host interaction will aid in the understanding of how infection develops in the healthcare setting. In addition, a discussion of the development of antibiotic resistance is warranted because of the substantial impact of resistant pathogens on the management of HAIs.
A healthy human body has several defenses against infection: the skin and mucous membranes form natural barriers to infection, and immune responses (nonspecific and specific) are activated to resist micro-organisms that are able to invade. The skin can effectively protect the body from most micro-organisms unless there is physical disruption. For example, the human papillomavirus can invade the skin, and some parasites can penetrate intact skin, but bacteria and fungi cannot . Other disruptors of the natural barrier are lesions, injury, or, in the healthcare setting, invasive procedures or devices.
In addition to breaks in the skin, other primary entry points for micro-organisms are mucosal surfaces, such as the respiratory, gastrointestinal, and genitourinary tracts. The membranes lining these tracts comprise a major internal barrier to micro-organisms due to the antimicrobial properties of their secretions. The respiratory tract filters inhaled micro-organisms, and mucociliary epithelium in the tracheobronchial tree moves them out of the lung. In the gastrointestinal tract, gastric acid, pancreatic enzymes, bile, and intestinal secretions destroy harmful micro-organisms. Nonpathogenic bacteria (commensal bacteria) make up the normal flora in the gastrointestinal tract and act as protectants against invading pathogenic bacteria. Commensal bacteria are a source of infection only if they are transmitted to another part of the body or if they are altered by the use of antibiotics .
The transmission of infection follows the cycle that has been described for all diseases, and humans are at the center of this cycle . In brief, a micro-organism requires a reservoir (a human, soil, air, or water), or a host, in which to live. The micro-organism also needs an environment that supports its survival once it exits the host and a method of transmission. Inherent properties allow micro-organisms to remain viable during transmission from a reservoir to a susceptible host, another essential factor for transmission of infection. The primary routes of transmission for infections are through the air, blood (or body fluid), contact (direct or indirect), fecal-oral route, food, animals, or insects. Once inside a host, micro-organisms thrive because of adherent properties that allow them to survive against mechanisms in the body that act to flush them out. Bacteria adhere to cell surfaces through hair-like projections, such as fibrillae, fimbriae, or pili, as well as by proteins that serve as adhesions . Fimbriae and pili are found on gram-negative bacteria, whereas other types of adhesions are found with both gram-negative and gram-positive bacteria. Receptor molecules in the body act as ligands to bind the adhesions, enabling bacteria to colonize within the body. The virulence of the micro-organism will determine whether only colonization occurs or if infection will develop. With colonization, there is no damage to local or distant tissues and no immune reaction; with infection, bacterial toxins that break down cells and intracellular matrices are released, causing damage to local and distant tissues and prompting an immune response in the host. Bacteria continue to thrive within a host through strategies that enable them to acquire iron for nutrition and to defend against the immune response. These virulence factors enhance a micro-organism's potential for infection by interrupting or avoiding phagocytosis or living inside phagocytes .
A healthcare environment increases the risk of infection for two primary reasons. First, it is likely that normally sterile body sites will become exposed, allowing pathogens to cause infection through contact with mucous membranes, nonintact skin, and internal body areas. Second, the likelihood of a susceptible host is high due to the vulnerable health status of patients. Especially in an era of decreased hospital stays and increased outpatient treatments, it is the sickest patients who are hospitalized, increasing the risk not only for infection to develop in these patients but also for their infection to be more severe and to be transmitted to others.
Infection is transmitted in a healthcare environment primarily through exogenous and endogenous modes. Exogenous transmission is through patient-to-patient or staff-to-patient contact. Patients who do not have infection but have bacterial colonization can act as vectors of transmission. Staff members can also act as vectors because of colonization or contamination. Endogenous infection occurs within an individual patient through displacement of commensal micro-organisms.
In general, the spread of infectious disease is prevented by eliminating the conditions necessary for the micro-organism to be transmitted from a reservoir to a susceptible host. This can be accomplished by:
Destroying the micro-organism
Blocking the transmission
Protecting individuals from becoming vectors of transmission
Decreasing the susceptibility of potential hosts
Antiseptic techniques and antibiotics will kill micro-organisms, and proper hand hygiene will block their transmission. Gloves, gowns, and masks remove healthcare workers from the transmission cycle by protecting them from contact with micro-organisms. Contact precautions and isolation techniques help patients avoid being vectors of transmission. Lastly, ensuring that patients and healthcare workers are immune or vaccinated can help decrease the availability of potential hosts.
The prevalence of drug-resistant micro-organisms has reached a critical level, and the inappropriate use of antibiotics is often cited as a primary cause of drug-resistant infections. As much as 50% of antimicrobial use is inappropriate . The prophylactic use of antibiotics preoperatively and the empiric use of antibiotics have helped bacteria to develop resistance in the healthcare setting. To meet the challenge of drug resistance, the management of antibiotic use has been a priority recommendation in guidelines developed for infection control programs in healthcare institutions, and review of the antibiotic formulary is required by institutions as part of compliance with Joint Commission standards [15,23,72,73]. (Guidelines for preventing drug-resistant infections in the healthcare setting are discussed in the Infection Control section.)
Although the inappropriate use of antibiotics is a major contributor to the development of drug resistance, other factors play an important role. These other factors include the natural ability of micro-organisms to adapt through genetic plasticity and rapid replication and the lack of antibiotic discovery and development over the past decades . For example, when the efficacy of antibiotics was first demonstrated in the late 1920s, their development and manufacture increased rapidly, and they began to be widely used (too widely, perhaps). However, over the next 40 years, no new class of antibiotics was developed, and the number of new antibiotics has decreased substantially since 1983 (Figure 1) . In 2009, 16 antimicrobial compounds were in late-stage clinical development (phase II or later); however, these compounds represent only incremental advances compared with currently available options, and few address the most commonly resistant pathogens . Only two new antibiotics were approved between 2009 and 2013, and the number of new antibiotics annually approved in the United States continues to decline. A 2013 IDSA report identified seven drugs in clinical development that were not included in the 2009 list, but indicated that these agents fell short of addressing the clinically relevant spectrum of resistance . Drug resistance typically emerges first in the healthcare setting, varies according to healthcare setting and geography, and subsequently extends to the community setting . The transmission and persistence of resistant strains of pathogens in a healthcare setting depends on several factors: availability of vulnerable patients, selective pressure from use of antimicrobial agents, number of patients with colonization of infection, and presence and adherence to prevention efforts .
Underlying disease and severity of illness
Transfer of patients from another institution, especially from a nursing home
Exposure to antimicrobial drugs, especially cephalosporins
Gastrointestinal surgery or transplantation
Exposure to invasive devices (urinary catheter, central venous catheter)
Antimicrobial-resistant pathogens have been reported to be the source of approximately 14% to 20% of HAIs, and these HAIs are associated with higher rates of morbidity and mortality and greater economic costs than antimicrobial-susceptible infections [39,79,80,81].
The most common drug-resistant HAI is MRSA, which emerged as a significant problem in the 1980s and increased steadily in prevalence, with a rate of approximately 59% of S. aureus infections in U.S. intensive care units (ICUs) in 2004 . Since that time, however, the rate of MRSA associated with HAIs has decreased, most likely because of increased preventive strategies [78,81]. Overall, the rate of HAIs attributable to antimicrobial-resistant pathogens has not changed substantially since 2010 . According to data on HAIs reported to the NHSN in 2009–2010, 20% of the infections were with antimicrobial-resistant phenotypes: MRSA (8.5%); vancomycin-resistant Enterococcus (3%); extended-spectrum cephalosporin-resistant Klebsiella pneumoniae and K. oxytoca (2%); Escherichia coli (2%); Enterobacter spp. (2%); and carbapenem-resistant Pseudomonas aeruginosa (2%) . The discovery of carbapenem-resistant Enterobacteriaceae as a new threat led the CDC to issue a guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in the healthcare setting [82,83].
Antimicrobial-resistant HAIs are associated with substantial morbidity and mortality compared with antimicrobial-susceptible HAIs, with longer hospital stays (excess of approximately 7 to 13 days), greater attributable mortality (up to 15%), and higher costs (additional $7,000 to $15,000) . Guidelines for the prevention and management of multidrug-resistant pathogens in the hospital setting have been developed by the CDC, SHEA, and IDSA, with the most recent guidelines focusing specifically on the treatment of MRSA [23,30,33,84]. More information on antimicrobial-resistant pathogens is given in the discussions of each type of HAI. In addition, prevention of MRSA infection is addressed in the Infection Control section, as prevention is an important aspect of a healthcare facility's infection control program.
In general, the sources of HAIs can be categorized as being related to environmental factors (air, water, architectural design), patient-related factors (age, degree of illness/immune status, length of hospital stay), and iatrogenic factors (invasive procedures, devices, and equipment).
Factors specifically related to the healthcare environment are not common causes of HAIs [15,85,86]. However, consideration should be given to the prevention of infection with environmental pathogens, such as fungi (e.g., Aspergillus), bacteria (e.g., Legionella species), or viruses (e.g., varicella) (Table 3). CDC guidelines provide clear recommendations for infection control measures according to several environment-related categories, including air (normal ventilation and filtration, as well as handling during construction or repair), water (water supply systems, ice machines, hydrotherapy tanks and pools), and environmental services (laundry, housekeeping). The infection control program of a facility has oversight of these measures.
ENVIRONMENTAL SOURCES OF PATHOGENS IN THE HEALTHCARE SETTING
|Water (tap and bath)||
Droplets containing micro-organisms can be transmitted in the air, causing infection in patients either directly or indirectly (through contamination of devices or equipment). Cleaning activities, such as sweeping, dry mopping, dusting, or shaking linen, can contribute to the transmission of airborne micro-organisms. Bacteria in the air primarily consist of gram-positive cocci from the skin, and they can be eliminated with appropriate ventilation and circulation of air . Many airborne viruses such as influenza and other respiratory viruses and measles do not carry far from the source; others, such as tuberculosis and varicella zoster, may be spread over long distances . The most common fungal spore to be transmitted through air is Aspergillus, which is carried through dust particles, can survive for long periods, and is easily inhaled . Under normal circumstances, the level of contamination with this airborne fungus' spores is not high enough to cause disease in otherwise healthy individuals. However, in the healthcare setting, the fungus causes respiratory infection, primarily pneumonia, in susceptible hosts.
The prevalence of infection with Aspergillus within a healthcare setting has been strongly associated with Aspergillus spore counts. Consequently, air conditioning systems with high-efficiency particulate air (HEPA) filters are needed to minimize contamination . HEPA filters are especially needed to prevent infection with Aspergillus in patients at high risk for infection due to a suppressed immune system. In one study, the risk of transplant-related mortality and overall mortality in the first 100 days after transplantation were significantly lower among patients treated in rooms with HEPA and/or laminar flow units than among patients treated in conventional isolation units . In these units, the air exchange rate should be high (more than 15 exchanges per hour), rooms should be tightly sealed, and the air pressure in the rooms should be positive in relation to the hallway [89,91,92]. HEPA filters are also used in the hoods in microbiology laboratories and pharmacies, laminar flow units in ICUs, and unidirectional flow units in operating room suites .
Maintaining a high quality of air in operating rooms is an essential factor in preventing postoperative infection. The number and movement of staff within the operating room create the primary sources of airborne bacteria. Other factors influencing airborne contamination include the type of surgery, the rate of air exchange, the initial quality of the air, the quality of the staff clothing and cleaning processes, and the level of compliance with infection control practices .
The CDC makes several suggestions about ventilation in the operating room in its guidelines for prevention of surgical site infections . The Level I recommendations include:
Maintain positive-pressure ventilation in the operating room with respect to the corridors and adjacent areas.
Maintain a minimum of 15 air changes per hour, of which at least three should be fresh air.
Filter all air, recirculated and fresh, through the appropriate filters per recommendations of the American Institute of Architects.
Introduce all air at the ceiling and exhaust near the floor.
Do not use ultraviolet radiation in the operating room to prevent surgical site infection.
Keep operating room doors closed except as needed for passage of equipment, personnel, and the patient.
Special care must be taken to protect patients during repair or renovation of a healthcare facility, as construction work can facilitate the spread of airborne organisms such as Aspergillus species . Some construction issues that contribute to the spread of infection include water-damaged building materials, disruption of duct work, open windows, and improper setting of fans or installation of filters .
The Joint Commission requires an inspection process for construction on a facility, and a risk assessment is part of that process . Risk factors to consider include the patient population, the extent and duration of the project, the impact of the project on mechanical systems, and whether space with construction will be occupied . A representative from a facility's infection control program should review any plans for construction to ensure that barriers are used as appropriate and patients, especially those with compromised immune systems, are moved to an area away from construction .
Water is a reservoir for several types of micro-organisms, including bacteria, fungi, and viruses, with viruses accounting for only a small percentage [85,94]. The quality of water within a healthcare setting must meet standards that vary according to use. Tap water must be safe to drink and use for baths (for hygiene and therapy) according to criteria dictated by local regulations and public health standards. The water supply to the healthcare facility can be disinfected by several methods, including chlorination, thermal eradication, ultraviolet light, and metal ionization .
The most common pathogen identified in tap water is P. aeruginosa . In one study, researchers evaluated the association between tap water from faucets in a surgical ICU and patients with colonization or infection with P. aeruginosa . The pathogen was found in 58% of water samples taken from individual faucets but was not identified in the main water supply. The genotypes of the micro-organism in 21 of the 45 patients were identical to those found in the tap water from the sink in the patient's room (15 patients) or in the adjacent room (6 patients). According to epidemiologic analysis, transmission of the pathogen had occurred from faucet to patient as well as from patient to faucet. P. aeruginosa is also the primary bacterial pathogen found in bath water . The effect of infection with P. aeruginosa may be mild, as in folliculitis and external otitis, but wound infection may be more severe. Greater morbidity is associated with infection in individuals who have a compromised immune system or who have another health condition, such as diabetes .
Legionella, which causes infection of the respiratory tract, is another micro-organism commonly found in tap water and bath water. The highest concentrations of Legionella are found in areas of water distribution systems (hot water storage, cooling towers, condensers), where it colonizes . Infection with Legionella is transmitted only through water, not through person-to-person contact. Inhalation of contaminated water droplets from shower heads or faucet aerators may cause disease . In addition, high humidity levels in a room (through mists produced by respiratory equipment, for example) may promote the growth of Legionella and molds .
WHO suggests that there is potential risk for HAIs if tap water is used for such purposes as ice machines or devices for washing eyes or ears, or for cleaning equipment . Point-of-use filtration may help to reduce the risk of HAIs related to water . Ducts, humidifiers, dehumidifiers, and other areas of a ventilation system should be kept clean and dry, as micro-organisms can colonize in water that accumulates in these areas . Patients at high risk for infection should not be exposed to hospital water and sterile water should be used instead .
Another factor in the transmission of infection in the healthcare setting is the architectural design of the facility, and the AHRQ lists "good hospital design principles" as one of its 10 patient safety tips for hospitals . When the American Institute of Architects and the Facility Guidelines Institute updated its Guidelines for Design and Construction of Hospital and Health Care Facilities in 2006, they set single-bed private rooms as the minimum standard for new hospital construction . This new standard was based on a literature review that showed, in part, that private rooms have been associated with lower rates of HAIs . Among the benefits of single-patient rooms compared with multibed rooms are decreased risk of infection through contaminated surfaces (e.g., blood pressure cuffs, privacy curtains); availability of private bathrooms; greater ease of cleaning and decontamination; increased likelihood of appropriate hand hygiene between rooms (rather than between beds within a single room); and decreased risk of prolonged hospital stays and patient transfers, all of which are risk factors for HAIs .
The WHO guidelines on infection control refer to "architectural segregation" according to risk . Four areas of a healthcare facility are defined, with administrative sections considered as low-risk areas; regular patient wards as moderate-risk areas; ICUs, burn units, or isolation units as high-risk areas; and operating rooms as very high-risk areas. The WHO and others have recommended that traffic flow should be limited in higher risk areas .
The type of sink and the placement of sinks throughout a healthcare facility have been of critical concern because of the substantial role of handwashing in reducing the transmission of infection. As a result, sinks have been placed within easy access in each patient room. However, it is unclear that such placement promotes better hand hygiene, with no long-term clinically significant improvement in handwashing found when sinks are placed near points of clinical activity .
With the advent of alcohol-based handrub solutions as more effective hand hygiene, the placement of handrub dispensers has become more important than the placement of sinks . The CDC guidelines on hand hygiene recommend placing dispensers in convenient locations, such as at the entrance of each patient room or at the bedside.
Patient-related risk factors for HAIs include age, general health status, and the type of procedure to be carried out, and risk can be classified as minimal, medium, or high . Patients are at minimal risk if they have no significant underlying disease, have an intact immune system, and will not undergo an invasive procedure. Medium risk is assigned to older patients who are susceptible to disease for a variety of reasons, including decreased immune function, comorbid conditions, and low nutritional status. Medium risk also refers to patients who are to have a nonsurgical invasive procedure, such as a peripheral venous catheter or a urinary catheter.
Advances in medical treatments have led to longer lives for individuals of all ages who have had organ transplantation, cancer, or infection with human immunodeficiency virus (HIV), and their compromised immune system puts them at high risk for HAI. High risk is also assigned to patients with multiple trauma or severe burns, or those who have surgery or an invasive procedure that is considered to be high risk, such as endotracheal intubation or insertion of a central venous catheter.
The primary iatrogenic factors contributing to the development of HAIs are devices (nonimplanted and implanted) and invasive procedures. As noted, the four most common HAIs—catheter-associated urinary tract infection, intravascular device-related bloodstream infection, surgical site infection, and pneumonia (ventilator-associated and hospital-acquired)—are related to the use of invasive devices or invasive procedures.
HAIs have been associated with several types of devices and equipment unique to healthcare facilities. The Spaulding classification, developed in 1968, is widely used to categorize devices according to their associated risk of infection . The system includes three categories:
Critical: A device that enters normally sterile tissue or the vascular system
Semicritical: A device that comes into contact with intact mucous membranes and does not ordinarily penetrate sterile tissue
Noncritical: A device that does not ordinarily touch a patient or touches only intact skin
Most HAIs can be attributed to devices in the critical and semicritical categories, including intravascular catheters, surgical drains, urinary catheters, and endoscopic instruments . Discussion here is limited to endoscopic instruments, as infections related to the other devices are addressed in detail later. In general, the transmission of pathogens on endoscopic devices has been attributed to noncompliance with appropriate reprocessing (cleaning, disinfection, sterilization, and drying) [16,31,101,102]. In particular, appropriate drying has been overlooked as an integral component of reprocessing, and guidelines have been inconsistent in recommendations on drying .
Bronchoscopes and gastrointestinal endoscopes are the primary diagnostic scopes used in healthcare settings. Both types of devices are associated with a low risk of infection transmission. Approximately 500,000 flexible bronchoscopies are done in the United States each year [16,104]. Few studies, however, have been carried out to evaluate the risk of infection; nosocomial infection related to bronchoscopy is difficult to detect and is likely under-recognized and under-reported . In 2003, there were two reports of multiple pseudoinfections and true infections, primarily with P. aeruginosa, associated with bronchoscopes that had been reprocessed according to current standards [106,107]. However, in both reports, loose fittings over the valve stem for the working channel of the bronchoscope were thought to have prevented effective mechanical cleaning and disinfection . Overall, the pathogens associated with bronchoscopy-related infection have been P. aeruginosa, Serratia marcescens, nontuberculous mycobacteria, and environmental fungi . In 2014, the U.S. Food and Drug Administration (FDA) received 50 medical device reports that mentioned infection or device contamination associated with reprocessed flexible bronchoscopes . During the course of investigating these reports, the FDA identified two recurrent themes that contributed to device contamination or device-associated infection: failure to meticulously follow the manufacturer's instructions for reprocessing (e.g., failure to perform thorough manual cleaning before high-level disinfection), and continued use of devices, despite integrity, maintenance, and mechanical issues (e.g., persistent channel kinks or bends).
More studies have evaluated the risk of infection associated with gastrointestinal endoscopy, which is performed on approximately 10 to 20 million people each year . The American Society for Gastrointestinal Endoscopy (ASGE) estimates that infectious organisms are transmitted in 1 of 1.8 million gastrointestinal endoscopies . Furthermore, all instances of infection during endoscopy have been the result of noncompliance with established guidelines for reprocessing of endoscopy equipment, highlighting the importance of adhering to these recommendations [31,108,109,110].
As with bronchoscopy, the pathogen with the highest rate of transmission associated with gastrointestinal endoscopy is P. aeruginosa [108,110]. As is true for other pathogens associated with endoscopy, infection with P. aeruginosa has resulted from nonadherence to reprocessing guidelines; however, this pathogen differs from the others because of its predilection for a moist environment. Many cases of infection with P. aeruginosa have been linked to the water supply to the endoscope and to failure to completely dry the endoscope channels with a 70% alcohol solution and forced air [103,108,110]. Salmonella species have also been associated with endoscopy, but no cases have been reported since the publication of the 1988 guidelines for standardized cleaning and disinfection of the devices [108,110]. Infection with Helicobacter pylori has also been related to suboptimal cleaning and disinfection . Low rates of hepatitis B and C virus transmission have been reported, and most cases of infection with hepatitis C were found to be related to the inappropriate use of multiple-dose vials and/or syringes rather than to the endoscope itself [31,108].
Noncritical devices are often overlooked by healthcare workers as vectors for infection. These devices include diagnostic equipment, stethoscopes, and other commonplace items. A systematic review of 23 studies found bacterial contamination of 87% of sampled healthcare equipment, primarily stethoscope membranes, as well as diagnostic ultrasound equipment, otoscopes, and auriscopes . The organisms found on healthcare equipment have primarily been S. aureus, including MRSA; Pseudomonas spp.; Acinetobacter spp.; and Pasteurella spp. . Washing stethoscopes with either an ethanol-based cleanser or isopropyl alcohol pads significantly reduces bacterial growth, even that of MRSA [113,114,115].
Contamination of therapeutic ultrasound transducer heads and ultrasound gels were evaluated in another study, and the rate of contamination was 27% for the heads and 28% for the gels . The transducer heads had low levels of contamination, and most of the micro-organisms were normal flora; however, high levels of contamination were found in the gels, and the micro-organisms included such pathogens as Stenotrophomonas maltophilia, S. aureus, Acinetobacter baumannii, and Rhodotorula mucilaginosa. In two other studies, contamination of dermatoscopes was evaluated. One study indicated colonization of only nonpathogenic bacteria and the other showed that use of an alcohol-based antibacterial gel as immersion fluid yielded no bacterial growth [117,118].
Ward-based computer terminals have also been shown to have low levels of contamination. In a study of two hospitals, MRSA was found on one of 13 computer terminals in one hospital and on five of 12 in another hospital. The rate of MRSA transmission was significantly higher at the hospital with the greater number of contaminated computers .
In summary, a high rate of micro-organism colonization has been found on equipment within the hospital setting, but contamination is usually at low levels and the risk of direct infection is low. In general, the findings of studies have suggested that adequate cleaning of equipment can prevent as many as one-third of HAIs .
Surgically implanted devices are a major source of HAI, and the development and use of intracardiac devices, orthopedic implants (prostheses and fixation devices), neurosurgical devices, cochlear implants, and breast and penile implants have increased over the past several years. The most common complication with all of these devices is infection [120,121,122]. The prevalence of infection associated with these devices varies, with the prevalence highest for left ventricular assist devices (Table 4) . Orthopedic implants, such as joint prostheses and fracture fixation devices, are associated with the lowest rate of infection, but reported mortality rates have been as high as 18% .
|Type of Device||Prevalence||Probable Cause||Typical Duration to Occurrence after Implantation||Most Common Micro-organisms||Signs and Symptoms||Diagnosis||Treatment|
|Left ventricular assist devices||25% to 50%||Biofilm formation||Within 2 to 6 weeks||Methicillin-resistant staphylococcal spp., Pseudomonas spp., Klebsiella spp., E. coli, Enterobacter spp., Proteus spp., Serratia spp., Candida spp., Enterococcus spp.||Signs of poor healing, localized inflammation, pocket abscess, frank sepsis, new and persistent drainage||Blood cultures||Empiric therapy with vancomycin and an anti-pseudomonal agent (ceftazidime or ciprofloxacin) or empiric antifungal therapy|
|Cerebrospinal fluid (CSF) shunts||10%||Bacteria originating from patient's skin introduced at time of operation||Within 30 days||Staphylococcus epidermidis (40% to 45%), S. aureus (25%), Klebsiella spp.,Enterobacter spp., Pseudomonas aeruginosa, Acinetobacter baumanii, Corynebacterium spp., Propionibacterium spp., and streptococci/enterococci||Fever, focal pain, ventriculitis with lethargy and malaise (proximal shunts), infected intraperitoneal fluid cysts, or frank peritonitis (distal shunts)||CSF analysis (cell count, glucose, protein), gram stain, culture; abdominal ultra-sonography (distal shunts)||Antimicrobial agent effective against noted micro-organisms, modified with results of culture; removal of shunt|
|Prosthetic cardiac valves||3% to 5.7%||Contamination of the valve at time of implantation or transient bacteremia||Within 60 days (early)||Coagulase-negative staphylococci, specifically methicillin-resistant S. epidermidis, S. aureus||Fever, new or changing regurgitant murmurs, CHF, shock, cardiac conduction disturbances on EKG||Blood cultures, transesophageal echocardiography||Delayed antibiotic therapy until results of culture available (if subacute course and hemodynamically stable); empiric antibiotic therapy with vancomycin, gentamicin, rifampin (evidence of significant valve dysfunction); valve replacement (new or increasing murmurs, severe CHF, persistent fever)|
|Penile implants||2% to 8%||Contamination at time of implantation||Not available||S. epidermidis||Erythema, induration, tenderness, fever, discharge, device extrusion, prosthesis-associated pain||Culture of specimen from the operative site||Empiric antibiotic therapy with ciprofloxacin or a cephalosporin for 10 to 12 weeks; removal of implant if pain persists or recurs after antibiotic treatment or if purulent discharge|
|Cochlear implants||1.7% to 3.3%||Contamination at time of implantation||Within 30 to 90 days||S. aureus, Streptococcus pneumoniae, Haemophilus influenzae||Skin flap necrosis, wound dehiscence, wound infection||Not available||Antibiotic therapy, incision and drainage, local wound care; removal of device if extrusion of device or implant-related sepsis|
|Transvenous permanent pacemakers/ automatic implantable cardioverter defibrillators||1% to 7%||Intraoperative contamination of the device or the pocket (early); contamination of pocket as a result of erosion of generator/ defibrillator through skin (late)||Within 30 days (early); within 60 days (late)||S. aureus, Propionibacterium acnes, Micrococcus spp., E. coli, Klebsiella spp.,Enterobacter spp., Serratia spp. (early); coagulase-negative staphylococci (late)||Erythema, pain, warmth at site ("pocket cellulitis"), draining sinus tract or erosion of overlying skin, systemic symptoms (fever, chills, malaise, nausea)||Blood cultures, transesophageal echocardiography||Prolonged antibiotic therapy, removal of all hardware; empiric therapy with vancomycin, gentamicin, or rifampin|
|Breast implants||1.7% to 2.5%a||Not available||Within 2 to 4 weeks||S. aureus, peptostreptococci, Clostridium perfringens||Erythema, edema, poor healing, purulent discharge, inflammatory symptoms (breast or axillary pain, paresthesia of upper extremity)||Wound or fluid culture||Empiric antibiotic therapy, local debridement|
|Orthopedic implants||<1% to 2%||Intraoperative contamination (early and late)||<2 to 4 weeks (early); >30 days (late)||S. aureus, coagulase-negative staphylococci, Propionibacterium spp. (early and late)||Persistent pain, fever, evidence of wound infection (early); loosening of prosthesis, sinus tract formation with discharge||Joint aspiration, complete blood count, erythrocyte sedimentation rate, C-reactive protein, imaging||Surgical exploration and debridement followed by empiric antibiotic therapy|
|aAfter augmentation mammoplasty; rates may be higher after mastectomy.|
Many implanted device-related infections are caused by contamination during insertion, but these infections are not always the result of micro-organisms transmitted in the healthcare setting. Rather, bacteria (and sometimes fungi) colonize by adhering to the surface of the implant through the development of a biofilm . Biofilms present another challenge in managing infection; biofilms provide bacteria with an extremely high level of resistance to antimicrobial agents. In fact, biofilms can tolerate antibiotic concentrations of 10 to 1,000 times of that needed to destroy free-floating (planktonic) bacteria . Many bacteria, including P. aeruginosa, are capable of existing in a planktonic state .
The CDC defines implanted device-related HAIs as those occurring within 1 year after implantation of a device, and the typical interval between implantation and infection varies according to the type of implant . For some implants, early and late infections differ with respect to etiology and the causative micro-organisms .
The treatment of infections related to these devices depends on the severity of the infection and the patient's underlying condition. A multidisciplinary approach involving antibiotic therapy and surgical intervention (either debridement or removal of the device) can have a substantial impact on morbidity and mortality. For example, prosthetic valve endocarditis is associated with mortality rates of 42% to 100%, but the rate can be decreased 20-fold through an approach that combines medical and surgical therapy rather than medical therapy alone . Empiric antibiotic therapy is usually appropriate once specimens have been obtained for culture, with the antibiotic agent chosen on the basis of the most common micro-organisms.
HAI is clearly defined by the CDC in the NHSN as a "localized or system condition (1) that results from adverse reaction to the presence of an infectious agent(s) or its toxin(s); and (2) that was not present or incubating at the time of admission to the hospital" . Thus, an infection is considered to be healthcare associated if it is unrelated to the admitting diagnosis and develops within 48 hours after admission. The CDC notes that an infection should be considered healthcare associated if it is thought that the infection was acquired in the hospital but did not become evident until after discharge . The diagnosis of infection is made on the basis of a combination of clinical findings and the results of laboratory studies or other diagnostic testing . The NHSN provides comprehensive details about the criteria for infection at 13 major anatomic sites and has developed clinical and biologic criteria for 48 specific sites or types of infection . The WHO has simplified the criteria to facilitate infection control in healthcare institutions with limited resources .
The rates of the five most common HAIs and the percentage each infection accounts for among all HAIs vary according to several factors, including time, geography, healthcare setting (including specific units within a hospital), and the data source. In general, catheter-related urinary tract infections are the most common, representing nearly one-third of all HAIs, and are the least costly; intravascular device-related bloodstream infections tend to be the most costly (in dollars); and ventilator-associated pneumonia is associated with the highest number of deaths (Table 5) [1,2,29,78,81,124,125,126,127,128,129,130]. Other HAIs defined in the NHNS include infection of bones and joints; the central nervous system; the cardiovascular system; the eye, ear, nose, throat, or mouth; the lower respiratory tract (other than pneumonia); the reproductive tract; skin and soft tissue; and systemic infection. Many of these other HAIs develop as complications of surgically implanted devices .
CHARACTERISTICS OF THE MOST COMMON HEALTHCARE-ASSOCIATED INFECTIONS
|Infection||Proportion of All HAIs||Incidence||Costs|
|Excess Stay||Attributable Mortality||Mean Hospital Cost per Infection (U.S. Dollars)|
|Catheter-associated urinary tract infection||32%||20% to 40% of patients with an indwelling catheter||10 days||1%||$1,006|
|Surgical site infection||22%||1% to 3% of surgical patients||7 to 10 days||3% to 5%||$25,546|
|Central line-associated bloodstream infection||14%||1% of patients with a central line||10 to 20 days||35%||$36,441|
|Ventilator-associated pneumonia||15%||10% to 65% of intubated patients||4 days||10% to 50%||$9,966|
|Healthcare-associated pneumonia (other than ventilator associated)||<1%||NA||NA||NA||NA|
|Clostridium difficile-associated diarrhea||Not available||30% of hospitalized adults with diarrhea||3 to 6 days||6% to 7%||$9,000–$11,000|
|NA = Not available.|
The risk factors for each of these HAIs have been delineated in many studies (Table 6) [19,78,131,132,133,134,135,136,137,138]. Yet, predicting which patients are at risk can be difficult. In one study, physicians in a surgical ICU were asked to assess at admission the individual risk of major HAI during the patient's stay in the unit. The investigators found that the physicians could not accurately predict risk, with positive predictive values that ranged from 8.4% to 14.5% and negative predictive values that ranged from 92.1% to 100% .
RISK FACTORS FOR HEALTHCARE-ASSOCIATED INFECTIONS
|Infection||Patient-Related Factors||Iatrogenic Factors|
|Urinary tract infection||
|Surgical site infection||
|Central line-associated bloodstream infection||
|Hospital-acquired pneumonia (not associated with a ventilator)||
|Clostridium difficile-associated diarrhea||
|ASA = American Society of Anesthesiologists.|
HAIs are predominantly caused by bacteria. Of the 81,139 pathogens (69,475 HAIs) reported to the NHSN between January 2009 and December 2010, 90% were bacteria and 10% were fungi . Approximately 82% of the reported pathogens belonged to one of eight main pathogen groups :
S. aureus (16%)
Enterococcus spp. (14%)
E. coli (12%)
Coagulase-negative staphylococci (11%)
Candida spp. (10%)
Klebsiella spp. (8%)
P. aeruginosa (8%)
Enterobacter spp. (5%)
The micro-organisms causing HAIs vary according to several factors, including the type of infection; in the overviews of the HAIs that follow, the most common micro-organisms specific to each infection are noted. Infectious agents also vary among healthcare facilities and even units within a single institution. Knowledge of trends in the pathogens responsible for HAIs is important in determining appropriate empiric therapy. This information changes frequently, and healthcare professionals should remain up-to-date with the pathogens identified in their own healthcare facilities and even on specific units within the facility. The IDSA/SHEA recommends computer-based surveillance (level II, B) as part of an overall antimicrobial stewardship program .
The IDSA defines a catheter-associated urinary tract infection as an infection occurring in a patient with an indwelling urinary catheter either currently in place or in place within the previous 48 hours . Approximately 15% to 25% of inpatients will have a urinary catheter inserted at some time during the hospital stay, and a urinary tract infection will develop in 20% to 40% of them [20,29]. The risk of infection varies from 3% to 8% per day when an indwelling catheter is in place . According to 2012 data from the NHSN, there were 4.7 to 5.3 catheter-associated urinary tract infections per 1,000 catheter-days . NHSN data show a 6% increase in catheter-associated urinary tract infections between 2009 and 2013, although initial data from 2014 indicate that these are beginning to decline . Of the 722,000 estimated HAIs in U.S. acute care hospitals in 2011, approximately 93,300 were catheter-associated urinary tract infections .
The duration of catheterization is the most important risk factor for infection . Studies have shown that catheterization for more than 2 days is a significant risk factor for urinary tract infection as well as increased 30-day mortality . Other risk factors for catheter-related urinary tract infection include no treatment with systemic antimicrobial agents, positive results on culture of the urethral meatus, microbial colonization of the urinary drainage bag, insertion of the catheter outside the operating room, and nonadherence to guidelines for appropriate catheter care. Patient-related risk factors include female gender, older age, diabetes, and an elevated level of serum creatinine at the time of catheterization .
Urinary tract infections can be caused by both endogenous and exogenous transmission. Normal flora from the gastrointestinal tract can spread to the urinary tract, or pathogens can be transmitted by caregivers carrying out tasks related to the catheter or drainage bag. Occasionally, pathogens are transmitted through urologic equipment that has not been adequately disinfected. Extraluminal ascension of bacteria along the catheter-urethral mucosa interface is the most common pathway of infection, accounting for approximately two-thirds of infections .
According to NHSN data for 2011, the most common cause of catheter-related urinary tract infections is E. coli (27.7%), followed by K. pneumonia/oxytoca (23.1%), Enterococcus faecalis (16.9%), and P. aeruginosa (10.8%) . Infections related to short-term catheterization is usually caused by a single agent, whereas infections related to long-term catheterization (30 days or more) is typically caused by multiple pathogens. P. mirabilis, Morganella morganii, and P. stuartii are additional common pathogens in infections related to long-term catheterization .
With regard to antimicrobial-resistant pathogens, the percentage of S. aureus infections resistant to oxacillins decreased in 2009–2010 (59% vs. 65% in 2007–2008) . The percentage of Enterococcus faecium resistant to vancomycin increased, to 83% (from 80% in 2007–2008), as did the percentage of vancomycin-resistant E. faecalis (approximately 8% vs 6% in 2007–2008). Multidrug-resistant Enterobacter spp. also increased, from 3% in 2007–2008 to nearly 5% in 2009–2010 .
The CDC updated its evidence-based guidelines for preventing catheter-associated urinary tract infections in 2009 (Table 7), and the IDSA published evidence-based clinical practice guidelines on the prevention, diagnosis, and treatment of catheter-associated urinary tract infections in 2010 [20,29]. According to both guidelines, the most important principles for prevention are:
Limit the use of indwelling urinary catheters.
Use aseptic technique and sterile equipment when inserting a catheter.
Secure the catheter properly.
Use a closed sterile drainage system.
Maintain unobstructed urine flow.
Remove the catheter as soon as feasible.
SUMMARY OF LEVEL I RECOMMENDATIONS FROM THE CENTERS FOR DISEASE CONTROL AND PREVENTION (CDC) FOR THE PREVENTION OF CATHETER-ASSOCIATED URINARY TRACT INFECTIONa
|Appropriate Urinary Catheter Use|
|Proper Techniques for Urinary Catheter Insertion|
|Proper Techniques for Urinary Catheter Maintenance|
|Quality Improvement Programs|
|Implement quality improvement programs or strategies to enhance appropriate use of indwelling catheters and to reduce the risk of catheter-associated urinary tract infections based on a facility risk assessment. The purposes of quality improvement programs should be to: ensure appropriate utilization of catheters; identify and remove catheters that are no longer needed (e.g., daily review of their continued need); and ensure adherence to hand hygiene and proper care of catheters.|
|aLevel I recommendations are supported by high-to-moderate quality evidence suggesting net clinical benefits or harms, or by low-quality evidence suggesting net clinical benefits or harms, or an accepted practices supported by low-to-very low quality evidence.|
As with prevention of all HAIs, handwashing is an essential element of aseptic technique and care of patients with catheters. In addition, healthcare staff should be educated and trained in proper techniques of catheter insertion and care.
Alternatives to indwelling catheters have been evaluated as an approach to preventing catheter-related urinary tract infections. The IDSA guidelines note that a suprapubic catheter may be considered as an alternative to short-term catheterization (level III, C), but use of this type of catheter is limited because an invasive procedure is needed for insertion . Intermittent catheterization may also be considered as an alternative to short-term (level I, C) or long-term (level III, A) catheterization, and, for men who have minimal postvoid residual urine, condom catheterization can be considered as an alternative to short-term (level II, A) or long-term (level II, B) catheterization in those who are not cognitively impaired .
The use of catheters coated with an antimicrobial surface has been evaluated, especially those coated with silver, a highly effective antibacterial substance. In one study, the addition of silver did not reduce the incidence of bacteriuria when compared with silicone-based, hydrogel-coated urinary catheters with and without silver impregnation . One meta-analysis (12 trials; 13,392 patients or catheters) showed that antimicrobial-coated catheters prevented or delayed the onset of bacteriuria in select patients, but the magnitude of the effect varied substantially according to several variables, including catheter type and publication year . A subsequent systematic review (eight studies) found a favorable trend toward a lower rate of infection with silver alloy (vs uncoated) catheters, but the quality of some studies was poor and there was significant heterogeneity among the studies . The 2009 CDC guidelines state that antimicrobial/antiseptic-impregnated catheters can be considered if the rate of catheter-associated urinary tract infections does not decrease after a comprehensive prevention strategy has been implemented . The guidelines add that further research is needed to determine the effect of these catheters in reducing the risk of symptomatic infection, their inclusion among the primary interventions, and the patient populations most likely to benefit from them .
Similarly, the IDSA states that catheters coated with an antimicrobial surface may be considered to reduce the risk of infection for patients who are to have short-term catheterization (level II, B), but notes that the data on the effectiveness of this strategy are insufficient .
The IDSA guidelines note several prevention strategies that should not be used routinely, primarily because of insufficient data :
Systemic antimicrobials in patients with short-term (level III, A) or long-term (level II, A) catheterization
Antimicrobials or antiseptics added to the drainage bag (level I, A)
Catheter irrigation with antimicrobials (level II, A) or normal saline (level II, B)
Enhanced meatal care (level I, A)
Methenamine salts (although prophylaxis with methenamine salts may be considered after gynecologic surgery for women who have a catheter for less than 1 week) (level 1, C)
Catheter-associated urinary tract infections are classified by both the CDC and the IDSA as symptomatic urinary tract infection, asymptomatic bacteriuria, or other infection of the urinary tract, and the results of urinalysis and urine cultures (using a clean catch technique or catheterization) are necessary for diagnosis [29,123].
The IDSA notes that catheter-associated urinary tract infection is defined by the presence of signs or symptoms compatible with a urinary tract infection with no other identified source, and at least one bacterial species at a count of ≥103 cfu/mL in one urine specimen (level III, A) . This threshold differs from that defined by the CDC (≥105 cfu/mL), which is intended for infection control surveillance rather than detection of infection in an individual patient . In addition, the 2009 CDC guidelines define the criteria for symptomatic catheter-associated urinary tract infection as symptoms plus a positive urine culture at the threshold of ≥105 cfu/mL; if the urine culture result is between ≥103 and ≤105 cfu/mL, a positive urinalysis is needed to meet the diagnostic criteria .
Urine specimens for culture should not be obtained from the drainage bag; instead, a sample should be taken through the catheter port with use of aseptic technique . If there is no port, a needle and syringe can be used to puncture the catheter tubing and collect the specimen . For patients with a long-term indwelling catheter, the IDSA recommends replacing the catheter and collecting the specimen from the newly placed catheter .
Signs and symptoms suggestive of catheter-associated urinary tract infections include fever (new or worsening), flank pain, hematuria, pelvic discomfort, altered mental status, and malaise or lethargy not attributable to another cause; among patients without a current indwelling catheter, dysuria, urgency, and frequent urination are other symptoms . However, studies have shown that the classic symptoms of urinary tract infection are uncommon among patients with a catheter-associated infection . Pyuria is not diagnostic of catheter-associated urinary tract infection in patients with an indwelling catheter .
Asymptomatic bacteriuria is defined as the presence of significant bacteriuria with no signs or symptoms referable to the urinary tract .
Most catheter-associated urinary tract infections are actually cases of asymptomatic bacteriuria, and the IDSA recommends that these infections not be treated, as treatment has not been found to be beneficial [29,147,148]. The results of a urine culture will help guide treatment of symptomatic infections . For patients with a catheter in place, the catheter should be discontinued, if possible, and the urine specimen should be one that is voided midstream (level III, A) . If the catheter has been in place for more than 2 weeks and continued catheterization is necessary, the catheter should be replaced (level I, A) and the urine specimen should be collected from the newly placed catheter (level II, A) .
The IDSA guidelines do not recommend specific antibiotics for treatment but do recommend duration of treatment. Treatment for 7 days is recommended for patients in whom symptoms resolve promptly, and treatment for 10 to 14 days is recommended for patients in whom symptom response is delayed (level III, A) . The guidelines note that a 5-day regimen of levofloxacin may be considered for patients who are not severely ill (level III, B) .
It has been suggested that catheter-associated urinary tract infection is the most preventable HAI . Some studies have noted an increase in adherence to strategies to prevent catheter-associated urinary tract infection . The greatest adherence has been to guidelines for wearing gloves (97%), using appropriate hand hygiene (89%), and maintaining a sterile barrier (81%) . However, adherence to appropriate catheterization (in terms of both initial indication and duration) has been suboptimal, with studies demonstrating the following [29,143,150,151,152]:
No justifiable indication or an inappropriate indication (such as incontinence) for more than 50% of catheterizations
Lack of awareness of catheterization in 25% of physicians
Catheterization for more than 2 days among 50% of postoperative patients
No system for monitoring which patients had insertion of catheters in 56% of hospitals
No system for monitoring duration of catheterization in 74%
Policy for nurse-initiated discontinuation of catheterization in 10% of hospitals
The use of provider reminder systems—alone or in combination with base strategies—has a moderate strength of evidence . In one study, the combination of prompts in a computerized order-entry system and handheld bladder scanners led to an 81% decrease in the use of catheters and a 73% reduction in HAIs . For hospitals without order-entry systems, a handwritten reminder that the patient has a catheter has been effective in reducing the rate of infection . However, the use of reminder systems has been reported to be 9% to 12% [151,152].
Despite the lack of adherence to prevention guidelines, some progress has been made in reducing this HAI; the rate of symptomatic catheter-associated urinary tract infections decreased 19% to 67% between 2000 and 2007 in ICUs . Compliance with a nurse-driven evidence-based checklist led to a decrease in infections from 2.88/1,000 catheter days to 1.46/1,000 catheter days .
The CDC guidelines note that the following are effective elements of a quality improvement program :
A system of alerts or reminders to identify all patients with urinary catheters and assess the need for continued catheterization
Guidelines and protocols for nurse-directed removal of unnecessary urinary catheters
Education and performance feedback regarding appropriate use, hand hygiene, and catheter care
Guidelines and algorithms for appropriate perioperative catheter management (such as procedure-specific guidelines for catheter placement and postoperative catheter removal and protocols for management of postoperative urinary retention, such as nurse-directed use of intermittent catheterization and use of bladder ultrasound scanners)
According to National Hospital Discharge Survey data, 51.4 million inpatient surgical procedures were performed in 2010, creating a large population at risk for surgical site infections . The CDC healthcare-associated infection (HAI) prevalence survey found that there were an estimated 157,500 surgical site infections associated with inpatient surgeries in 2011 . Infection will develop postoperatively in approximately 2.6% of all patients who have surgery . The rate has decreased since the 1990s, but the lower rate is not thought to be an accurate representation because of the increased number of operations done on an outpatient basis; a decrease in the length of the postoperative hospital stay; and a wound infection incubation period of 5 to 7 days . This potential for underestimation of the number of surgical site infections is reflected in the findings of a study in which one-third of healthcare-associated wound infections were detected after the patient had been discharged . Surgical site infections are associated with extended lengths of stay, a high rate of readmissions, excess hospital costs, and a mortality rate of 3%, with a higher mortality rate reported for patients 70 years of age and older [2,160,161].
The number of surgical site infections reported to NHSN increased from 10,778 in 2007–2008 to 16,019 in 2009–2010 . However, the CDC reports a 19% decrease in surgical site infections related to 10 select procedures performed between 2008 and 2013 . The NHSN enables the CDC to monitor the distribution, etiology, and antimicrobial resistance pattern of infections in relation to the category of surgical procedure. The number of surgical site infections reported through NHSN increased from 10,778 in 2007–2008 to 16,019 in 2009–2010 . However, this may in part be a measure of improved surveillance, as the CDC reported a 19% decrease in infection associated with 10 select procedures performed between 2008 and 2013 . Table 8 shows the distribution of procedure-associated infections and common pathogens, by type of surgery, as reported to NHSN for 2009–2010 . Please note that the distribution percentage is primarily a reflection of the frequency (commonality) with which the given category of surgery is performed and not an indication of the actual rate, or risk, of infection from the specific procedure itself. It may be seen that, with the exception of abdominal procedures and transplant surgery, S. aureus (of which 44% of isolates were MRSA) accounted for the majority of these infections .
DISTRIBUTION OF SURGICAL SITE INFECTION AND MOST COMMON PATHOGENS ACCORDING TO TYPE OF SURGERY: DATA REPORTED TO THE NATIONAL HEALTHCARE SAFETY NETWORK, 2009–2010
|Type of Surgery||Percentage of Reported Surgical Site Infections||Most Common Pathogens|
|Orthopedic||41%||Staphylococcus aureus (47%), coagulase-negative staphylococci (14%), Streptococcus spp. (6%)|
|Abdominal||23%||Escherichia coli (19%), S. aureus (12%), Enterococcus faecalis (9%)|
|Cardiac||22%||S. aureus (31%), coagulase-negative staphylococci (17%), Pseudomonas aeruginosa (8%)|
|Obstetric/gynecologic||10%||S. aureus (20%), E. coli (13%), coagulase-negative staphylococci (9%)|
|Neurologic||2%||S. aureus (37%), coagulase-negative staphylococci (23%), Enterobacter spp. (7%)|
|Vascular||2%||S. aureus (33%), coagulase-negative staphylococci (8%), P. aeruginosa (8%), E. coli (8%)|
|Transplant||1%||Coagulase-negative staphylococci (16%), Enterococcus faecium (15%), E. coli (10%)|
The category of surgery and the duration of the procedure are factors affecting the incidence of post-procedure surgical site infection. The rate of infection by type of surgery varies across facilities; for example, in a multicenter Veterans Administration study, the overall rate of surgical site infection was 6%, with the highest rate (11.3%) following colorectal procedures and the lowest (1.3%) following orthopedic procedures .
Older age (≥65 years)
Poor nutritional status
Low serum albumin concentration
History of smoking
History of alcohol use disorders
Hypothermia, hypoxia, or hyperglycemia
Among the most common surgery-related factors are anesthesia score, duration of the operation, the use of drains, and inadequate aseptic technique . In a study to determine the influence of risk factors on complications after colorectal surgery, body mass index, duration of the operation, and the surgeon who performed the operation were the three most important factors influencing surgical site infections .
Surgical site infections arise from both endogenous and exogenous transmission. The microbial sources of surgical site infections vary according to the type of surgery, and the micro-organism reported as being the most common in 2009–2010 was S. aureus, which accounted for nearly half of all reported orthopedic surgical site infections . Other common causative pathogens were coagulase-negative staphylococci and E. coli .
Among the facilities reporting data on surgical site infections to the NHSN in 2009–2010, the percentage of resistant phenotypes was low for pathogens most often associated with surgical site infections . The percentage resistance for most pathogens decreased compared with data for 2007–2008; for example, 44% of S. aureus infections were resistant to oxacillins, a significant decrease from 48% in 2007–2008. The percentage of vancomycin-resistant E. faecium remained relatively stable (62% in 2009–1010), but the percentage of vancomycin-resistant E. faecalis increased from 4.6% to 6.2% in 2009–2010 . Also increasing were rates of resistance of E. coli to extended-spectrum cephalosporins (11%) and of P. aeruginosa to aminoglycosides (6%) .
The CDC guideline for preventing surgical site infections, published in 1999, addresses a wide variety of issues, including preoperative preparation of the patient, antisepsis of the surgical team, management of surgical personnel with colonization or infection, antimicrobial prophylaxis, ventilation, cleaning and disinfection of environmental surfaces, microbiologic sampling, sterilization of surgical instruments, surgical attire and drapes, asepsis and surgical technique, postoperative incision care, and surveillance. This guideline was updated in 2014 when the CDC published the Draft Guideline for Prevention of Surgical Site Infection [28,166]. The guidelines recommend a combination of key components as a strategy to prevent surgical site infection (Table 9).
LEVEL IA and IB RECOMMENDATIONS FOR THE PREVENTION OF SURGICAL SITE INFECTIONSa
|1999 Guideline||2014 Additions|
|Whenever possible, identify and treat all infections remote to the surgical site before elective operation, and postpone elective operations on patients with remote site infections until the infection has resolved. Do not remove hair preoperatively unless the hair at or around the incision site will interfere with the operation. If hair is removed, remove immediately before the operation, preferably with electric clippers. Adequately control serum blood glucose levels in all diabetic patients and particularly avoid hyperglycemia perioperatively. Encourage tobacco cessation. At minimum, instruct patients to abstain for at least 30 days before elective operation from smoking cigarettes, cigars, pipes, or any other form of tobacco consumption (e.g., chewing/dipping). Do not withhold necessary blood products from surgical patients as a means to prevent surgical site infection. Thoroughly wash and clean at and around the incision site to remove gross contamination before performing antiseptic skin preparation. Use an appropriate antiseptic agent for skin preparation.||
|Administer a prophylactic antimicrobial agent only when indicated, and select it based on its efficacy against the most common pathogens causing surgical site infection for a specific operation and published recommendations. Administer by the intravenous route the initial dose of prophylactic antimicrobial agent, timed such that a bactericidal concentration of the drug is established in serum and tissues when the incision is made. Maintain therapeutic levels of the agent in serum and tissues throughout the operation and until, at most, a few hours after the incision is closed in the operating room. Before elective colorectal operations, in addition to above recommendation, mechanically prepare the colon by use of enemas and cathartic agents. Administer nonabsorbable oral antimicrobial agents in divided doses||
|__||For patients with normal pulmonary function undergoing general anesthesia with endotracheal intubation, administer increased FiO2 both intraoperatively and postextubation in the immediate postoperative period. To optimize tissue oxygen delivery, maintain perioperative normothermia and adequate volume replacement.|
|Postoperative Incision Care|
|Protect with a sterile dressing for 24 to 48 hours postoperatively an incision that has been closed primarily. Wash hands before and after dressing changes and any contact with the surgical site.||__|
|aLevel I recommendations are supported by high-to-moderate quality evidence suggesting net clinical benefits or harms, or by low-quality evidence suggesting net clinical benefits or harms, or are accepted practices supported by low-to-very low quality evidence.|
Antimicrobial prophylaxis is the most important measure to prevent surgical site infection; the perioperative administration of an appropriate antibiotic substantially reduces the relative risk of a surgical site infection, and timing is crucial [15,28,166,167]. The CDC recommends that an appropriate prophylactic antibiotic be administered such that the serum concentration is optimal when the surgical incision is made and that antibiotic treatment be maintained until a few hours after the incision has been closed [28,166]. The CDC guidelines reference appropriate antibiotics on the basis of the type of surgery [28,166]. Meta-analyses have demonstrated lower rates of infection with a single-dose (long-acting) antibiotic and broader spectrum antibiotics, such as third-generation cephalosporins . However, a complication of perioperative antibiotic prophylaxis is an increased frequency of adverse events, the most serious of which is infection with C. difficile, and this risk may be higher in association with a broad-spectrum antibiotic .
Systematic reviews reported in the mid-2000s showed that two previously recommended measures for preventing postoperative infection have no effect on the rate of surgical site infection. One review involved six trials in which preoperative washing was evaluated in a total of 10,007 patients. There was no significant difference in the rate of surgical site infections when 4% chlorhexidine gluconate was compared with placebo or no washing . The other review involved 11 randomized controlled trials in which preoperative hair removal practices were evaluated. Comparison of razor, depilatory cream, or no hair removal showed no significant difference in the rate of surgical site infection [170,171]. However, when shaving was compared with clipping, there were significantly more surgical site infections after shaving. No difference was found in the rate of surgical site infections between clipping 1 day preoperatively or on the day of surgery. On the basis of these findings, preoperative antiseptic washing and shaving are no longer recommended.
Attention should also be directed at strategies to prevent surgical site infections with MRSA. The use of an MRSA prevention bundle—adherence to the guidelines for hand hygiene, decontamination of environment and equipment, active surveillance cultures, and contact precautions for patients with MRSA infection or colonization—led to significant decreases in the overall rate of surgical site infections in one study, with a 1% decrease in surgical site infections after cardiac surgery and a 65% decrease after orthopedic surgeries .
IDSA guidelines on the diagnosis and management of skin and soft tissue infections include a section on surgical site infections [158,173]. The guidelines note that the most reliable diagnostic information is the physical appearance of the site; local signs of infection include pain, swelling, erythema, and purulent drainage [158,173]. Clinical manifestations of a surgical site infection do not occur for at least 5 days postoperatively, with many infections not becoming apparent for as long as 2 weeks [158,173]. The IDSA notes that most postoperative fevers are not associated with a surgical site infection [158,173].
Surgical site infections are classified as superficial incisional, deep incisional, and organ/space infections. Strict criteria and standardized definitions are used in reporting infections and in surveillance programs [28,168]. The CDC described the criteria for each type of infection in its guidelines for the prevention of surgical site infections and defined the infections in the NHSN system according to this classification [28,123,174].
Infection occurs within 30 days after the operative procedure and involves only skin and subcutaneous tissue of the incision and at least one of the following:
Purulent draining from the superficial incision
Organisms isolated from an aseptically obtained culture of fluid or tissue from the superficial incision
At least one of the following signs or symptoms of infection: pain or tenderness, localized swelling, redness, or heat, and superficial incision is deliberately opened by surgeon, unless incision is culture-negative
Diagnosis of superficial incisional surgical site infection by the surgeon or attending physician
Infection occurs within 30 days after the operative procedure if no implant is left in place or within 1 year if implant is in place and the infection appears to be related to the operative procedure and involves deep soft tissues (e.g., fascial and muscle layers) of the incision and at least one of the following:
Purulent drainage from the deep incision but not from the organ/space component of the surgical site
Deep incision spontaneously dehisces or is deliberately opened by a surgeon when the patient has at least one of the following signs or symptoms: fever (>38 degrees Centigrade) or localized pain or tenderness, unless incision is culture-negative
Abscess or other evidence of infection involving the deep incision is found on direct examination, during reoperation, or by histopathologic or radiographic examination
Diagnosis of a deep incisional surgical site infection by a surgeon or attending physician
Infection occurs within 30 days after the operative procedure if no implant is left in place or within 1 year if the implant is in place and the infection appears to be related to the operative procedure and infection involves any part of the body, excluding the skin incision, fascia, or muscle layers, that is opened or manipulated during the operative procedure and at least one of the following:
Purulent drainage from a drain that is placed through a stab wound into the organ/space
Organisms isolated from an aseptically obtained culture or fluid or tissue in the organ/space
Abscess or other evidence of infection involving the organ/space that is found on direct examination, during reoperation, or by histopathologic or radiographic examination
Diagnosis of an organ/space surgical site infection by a surgeon or attending physician
Based on expert opinion, the IDSA recommends opening an infected surgical site, removing the infected material, and continuing dressing changes until the wound heals by secondary intention . Although treatment with antibiotics is commonly started when a surgical site infection is diagnosed, the IDSA notes that little evidence has supported this approach . A short course (24 to 48 hours) of antibiotics may be indicated for patients with a temperature higher than 38.5 degrees Centigrade or a pulse rate of more than 100 beats/min . The guidelines add that treatment is usually empirical but may be selected according to results of wound culture . IDSA offers guidance on the selection of antibiotics according to the operative site .
Single agents: ticarcillin/clavulanate, piperacillin/tazobactam, imipenem/cilastatin, meropenem, ertapenem
Combination agents: ceftriaxone/metronidazole, ciprofloxacin/metronidazole, levofloxacin/metronidazole, ampicillin-sulbactam/gentamicin ampicillin-sulbactam/ tobramycin
Oxacillin, nafcillin, cefazolin, cephalexin, SMX-TMP, vancomycin
Metronidazole/ciprofloxacin, levofloxacin, ceftriaxone
For surgical site infections after implantation of a joint prosthesis, the approach depends on the duration of infection, stability of the implant, antimicrobial susceptibility of the pathogen, and condition of the surrounding soft tissue . In this setting, rifampin has shown excellent activity against adherent staphylococci and may be useful in combination with beta-lactams, glycopeptides, fluoroquinolones, minocycline, trimethoprim, or fusidic acid .
The effect of prevention strategies—primarily the appropriate use of prophylactic antibiotics—on the rate of surgical site infection has been evaluated in several studies, and the results have been conflicting. For example, 56% adherence to this measure significantly reduced the incidence of surgical site infections in one study of patients who had colorectal surgery, with the rate decreasing from 22% to 3.5% . There was no significant difference in the rate of surgical site infection between compliant and noncompliant prophylactic antibiotics . In a retrospective review of 605 patients who had colorectal surgery with intestinal anastomosis showed that early administration of antibiotic prophylaxis and a nonstandard antibiotic were significantly associated with a greater risk of surgical site infection . However, the timely administration of prophylactic antibiotics did not improve the rate of surgical site infections among nearly 9,200 elective major surgeries (all types); the rate was 5% for patients who received timely antibiotics compared with 6% for patients who received antibiotic prophylaxis outside of the recommended time .
More recent studies have analyzed adherence to the Surgical Care Improvement Project (SCIP) quality measures, with analysis of individual measures as well as groups of measures. Some studies have indicated that an increase in compliance with SCIP measures leads to a decrease in the rate of surgical site infection; the rate decreased from nearly 26% to 16% in one study and in another study, increasing compliance with SCIP measures from 38% to 92% led to a decrease in the rate of superficial surgical site infections from 13% to 8% [49,179]. Among patients who had laparotomy related to trauma (gunshot wound, stab wound, or blunt trauma), adherence to SCIP measures related to antibiotic prophylaxis resulted in a significantly lower rate of surgical site infection (17% vs 33%) as well as a shorter hospital stay (14 vs 19 days), even after controlling for several factors .
However, these data have not been consistent. In a study of nearly 500 patients who had colorectal surgery, compliance with all SCIP measures improved—from 40% to 68%—but the rate of surgical site infections remained essentially the same (approximately 19%) . In addition, a retrospective review of 60,853 surgeries done over a 5-year period at 112 Veterans Administration (VA) hospitals showed that improving adherence to five SCIP measures did not significantly lower the odds of surgical site infection .
Many have been critical of the SCIP strategy, noting that the evidence has not indicated that adherence to these quality measures alone has had an effect on reducing the overall risk of surgical site infection . The quality measures do not factor in the skill of the surgeon, and other factors, such as state-of-the-art skin antisepsis and innovative antimicrobial technology, should be included in quality improvement programs [181,182].
Ways to help increase adherence to effective prevention strategies are the use of computerized standard orders for antibiotics, reminders and checklists, and auditing of the rates for individual physicians, with feedback . A study demonstrated that point-of-care prompts increased compliance with timely antibiotic prophylaxis from 62% to 92%, with a corresponding decrease in the incidence of surgical site infections, from 1.1% to 0.7% . In an extensive systematic review, there was moderate strength of evidence for the use of audit and feedback, with or without provider reminder systems, for improving adherence to appropriate timing of prophylactic antibiotics . The IHI how-to guide for the prevention of surgical site infection outlines practical steps to help healthcare professionals ensure that prevention strategies are carried out (Table 10) .
PRACTICAL STEPS IN FOLLOWING GUIDELINES TO PREVENT SURGICAL SITE INFECTIONS
|Appropriate Use of Prophylactic Antibiotics|
|Use preprinted or computerized standing orders specifying antibiotic, timing, dose, and discontinuation. Develop pharmacist- and nurse-driven protocols that include preoperative antibiotic selection and dosing based on surgical type and patient-specific criteria (e.g., age, weight, allergies, renal clearance). Change operating room drug stocks to include only standard doses and standard drugs, reflecting national guidelines. Reassign dosing responsibilities to anesthesia or holding area nurses to improve timeliness. Involve pharmacy, infection control, and infectious disease staff to ensure appropriate timing, selection, and duration. Verify administration time during "time-out" or preprocedural briefing so action can be taken if not administered.|
|Appropriate Hair Removal|
|Ensure adequate supply of clippers and train staff in proper use. Remove all razors throughout the hospital. Work with the purchasing department to ensure that razors are no longer purchased by the hospital. Use signs or posters as reminders. Educate patients about not shaving preoperatively.|
|Maintaining Adequate Glycemic Control|
|Implement one standard glucose control protocol (sliding scale or insulin drip). Regularly check preoperative blood glucose levels on all patients. Assign responsibility and accountability for blood glucose monitoring and control.|
|Maintaining a Warm Body Temperature|
|Use hats and booties on patients preoperatively. Use warmed forced-air blankets preoperatively, during surgery, and in the recovery room. Use warmed intravenous fluids. Use warming blankets under patients on the operating table.|
|Maintaining a Warm Body Temperature|
|Prevent hypothermia at all phases of the surgical process. Use hats and booties on patients perioperatively. Use warmed forced-air blankets preoperatively, during surgery, and in the recovery room. Use warmed intravenous fluids. Use warming blankets under patients on the operating table. Adjust engineering controls so that operating rooms and patient areas are not permitted to become excessively cold overnight, when many rooms are closed. Measure temperature with a standard type of thermometer.|
Pneumonia associated with healthcare facilities is classified in three categories: hospital-acquired, ventilator-associated, and healthcare-associated. Hospital-acquired pneumonia refers specifically to pneumonia that develops 48 hours after hospital admission (usually occurring postoperatively), and ventilator-associated pneumonia refers to pneumonia that develops 48 hours after tracheal intubation . Healthcare-associated pneumonia develops in individuals in healthcare facilities outside hospitals, such as long-term care facilities and outpatient settings.
Hospital-acquired pneumonia, also referred to as postprocedure pneumonia, is not included in most discussions of HAIs because it represents less than 1% of all such infections; although this type of pneumonia is not reportable to NHSN, 23 cases were reported in 2009–2010 . Still, hospital-acquired pneumonia can increase the length of stay by more than 1 week and is associated with increased mortality and financial cost .
The rate of ventilator-associated pneumonia is higher than that for hospital-acquired pneumonia, with a reported rate of 1 to 4 cases per 1,000 ventilator-days, and rates as high as 10 cases per 1,000 in some neonatal and surgical populations [17,187]. A total of 3,957 cases of ventilator-associated pneumonia were reported to NHSN in 2012 . The mortality rate of patients with ventilator-associated pneumonia is two to 10 times higher than those without the condition .
In a systematic review, the American College of Physicians found several patient-related and surgery-related factors that increased the risk of postoperative pulmonary complications. The most common patient-related factors were the presence of COPD and an age older than 60 years . Other significant factors were an American Society of Anesthesiologists (ASA) class 2 (defined as a patient with mild systemic disease) or higher, functional dependence, and congestive heart failure. Cigarette use was associated with a modest increase in risk, and obesity and mild or moderate asthma were not found to increase risk . Use of a PPI or histamine-2 receptor antagonist is also thought to be a risk factor . Surgery-related factors included prolonged duration of surgery (more than 3 to 4 hours), emergency surgery, and surgical site, with abdominal surgery, thoracic surgery, neurosurgery, head and neck surgery, vascular surgery, and aortic aneurysm repair being associated with the greatest risks .
The risk of ventilator-associated pneumonia correlates with the duration of intubation; the risk has been estimated to be 3% per day during the 5-day period after intubation, decreasing to 2% per day for days 5 through 10 and to 1% per day for longer durations .
Nearly half of all cases of ventilator-associated pneumonia develop within the first 4 days of mechanical ventilation . In addition to duration of ventilation, several other risk factors among adults have been identified, including a supine head position; use of a nasogastric tube, paralytic agents, or PPI or histamine-2 receptor antagonists; patient age; chronic lung disease; and head trauma [19,138]. In one study, ventilator-associated pneumonia was most frequently associated with ICU admission diagnoses of postoperative care, neurologic conditions, sepsis, and cardiac complications .
Most cases of hospital-acquired and ventilator-associated pneumonia are caused by aspiration of bacteria originating in the oropharynx or the stomach. Approximately 50% of all cases occur after surgery, with the highest risk associated with cardiac, abdominal, or orthopedic surgery. Cross-contamination, either through staff or equipment, is another cause . Viral and fungal pathogens are rare causes of hospital-acquired and ventilator-associated pneumonia in immunocompetent adults. Outbreaks of viral pneumonia may occur during influenza season, and influenza, parainfluenza, adenovirus, and respiratory syncytial virus (RSV) are involved in about 70% of those cases . Candida spp. and Aspergillus fumigatus may cause pneumonia in patients who have had organ transplantation or who have a compromised immune system and neutropenia.
Because of its low proportion of HAIs, data on hospital-acquired pneumonia is not collected through NHSN, but other studies have provided information on trends in the frequency of causative pathogens. Among adults with no previous antibiotic exposure, the most common bacterial causes of hospital-acquired pneumonia are S. aureus, S. pneumoniae, H. influenzae, E. coli, and K. pneumoniae [17,185,186,193]. Gram-negative bacilli resistant to first-generation cephalosporins also frequently develop in late-onset hospital-acquired pneumonia. For up to 40% of adults with previous antibiotic exposure, late-onset hospital-acquired pneumonia is caused by potentially multidrug-resistant pathogens, including P. aeruginosa, A. baumannii, and MRSA . In a study of more than 3,600 patients admitted to an ICU, Pseudomonas spp. was the cause of pneumonia in 25% of patients; MRSA in 18%; and Acinetobacter spp. in 6% . Other studies have shown that S. aureus is common among patients who are in a coma or have diabetes or renal failure; P. aeruginosa is common among patients who have had a prolonged stay in the ICU, have received prior antibiotics or corticosteroids, or who have structural lung disease; and Legionella is usually found in patients who have compromised immune systems .
In 2009–2010, the most common pathogens associated with ventilator-associated pneumonia in adults were S. aureus (24%) and P. aeruginosa (17%), followed by K. pneumonia/oxytoca (10%), Enterobacter spp. (9%), and A. baumannii (7%) . Almost half of all cases of ventilator-associated pneumonia are caused by infection with more than one pathogen . As with other HAIs, the percentage of resistant S. aureus has decreased (48% in 2009–2010 vs 52% in 2007–2008). The percentage of vancomycin-resistant E. faecium remained essentially the same (83% in 2009–2010), but the percentage of vancomycin-resistant E. faecalis increased from 6% in 2007–2008 to nearly 10% in 2009–2010 . Rates of resistant Klebsiella spp. were increased for extended-spectrum cephalosporins (24%), carbapenems (11%), and multidrug (13%) . Multidrug-resistant E. coli increased from 2% in 2007–2008 to 3% in 2009–2010 .
The CDC has published guidelines for the prevention of hospital-acquired and ventilator-associated pneumonia, with a focus on strategies to decrease or eliminate modifiable risk factors . These strategies are related to preoperative and postoperative care and measures to reduce the risk of transmission of etiologic pathogens. In addition, steps to prevent the spread of influenza virus are essential, especially during influenza season.
For many years, preventing postoperative pneumonia has been a part of initiatives to decrease complications among patients who have surgery. The Respiratory Risk Index was developed to classify patients as being at low, medium, or high risk for postoperative respiratory failure . The factors in the index include the complexity of the surgery, the ASA status, and comorbidities.
Smoking triples the risk for pulmonary complications after surgery, and smoking cessation for at least 8 weeks before surgery, when possible, is recommended for current smokers . The risk for complications in patients with respiratory disease or congestive heart failure can be ameliorated by optimum treatment before surgery (e.g., treatment with steroids for patients with COPD or asthma) .
Effective pain management after surgery can also help decrease the risk of pulmonary complications. For postoperative patients who are not mechanically intubated, the ability to cough and clear secretions is important for preventing pulmonary complications . The use of incentive spirometry and deep breathing exercises are recommended, especially for people at high risk for pulmonary complications, as are frequent coughing and early movement (in bed and/or walking) [24,137,186]. Fair evidence supports the selective (rather than routine) use of a nasogastric tube after abdominal surgery .
Two guidelines were developed to focus specifically on the prevention of ventilator-associated pneumonia; one was jointly developed by the SHEA and IDSA, and the other was jointly developed by the Canadian Critical Care Trials Group and the Canadian Critical Care Society [19,35]. In addition, prevention of ventilator-associated pneumonia is addressed in the CDC's guidelines on preventing healthcare-associated pneumonia and the American Thoracic Society (ATS)/IDSA guidelines on the management of healthcare-associated pneumonias [17,24]. The following multicomponent prevention strategy is suggested by these guidelines:
Assessment of readiness to extubate and daily interruptions of sedation
Elevation of the head of the bed
Daily oral care with chlorhexidine
Prophylaxis of peptic ulcer disease
Prophylaxis of deep vein thrombosis
Because of the increasing risk of infection as the duration of ventilation increases, the primary goal is to extubate patients as early as possible. Thus, assessment of the readiness for extubation and weaning protocols are key aspects in the preventive approach [17,193]. Daily interruption of sedation until the patient is awake has been shown to significantly decrease the number of days on mechanical ventilation, from 7.3 days to 4.9 days in one study . There are risks to this approach, such as the potential for increased pain, anxiety, and desaturation. However, the use of sedation interruption has been further demonstrated to reduce the complications of prolonged mechanical ventilation . The SHEA/IDSA guidelines recommend daily assessment of the readiness to wean and the use of weaning protocols .
Reducing the risk of aspiration and contamination with gastric secretions also helps to prevent the development of ventilator-associated pneumonia. The risk of aspiration has been significantly reduced by positioning the patient with the head of the bed at an angle of 30 to 45 degrees [19,196,197]. In one randomized controlled trial, there were 18% fewer cases of ventilator-associated pneumonia among intubated patients in the group assigned to the recumbent position (45 degrees) compared with the group assigned to the supine position . In another study, elevation of the head of the bed at 30 degrees was the most effective measure among a group of preventive interventions, resulting in a 52% variance in the rate of ventilator-associated pneumonia . Both the ATS/IDSA and SHEA/IDSA guidelines recommend maintaining the head of the bed at a 30- to 45-degree angle [17,35].
Oral care interventions have been suggested by some, in part because of an association between a high level of dental plaque and a high rate of colonization with aerobic pathogens, including S. aureus, gram-negative bacilli, and P. aeruginosa . Research has shown that oral decontamination with chlorhexidine leads to a significant reduction in the colonization of pathogens in the oropharynx; in most studies, the intervention has not had a significant effect on the rate of ventilator-associated pneumonia or associated mortality, but more recent studies showed significant decreases in the rate of ventilator-associated pneumonia [198,200,201,202]. Including tooth brushing with chlorhexidine does not seem to add benefit . Regular oral care with an antiseptic solution or chlorhexidine is recommended in the ATS/IDSA and SHEA/IDSA guidelines [17,35].
Prophylaxis of peptic ulcer disease has evolved with some conflicting views. Antacids, histamine-2 antagonists, and sucralfate have been traditionally given to patients receiving mechanical ventilation to prevent the formation of ulcers. However, reducing the amount of gastric acid can increase the risk of colonization of gram-negative bacilli in the stomach. As a result, WHO recommended avoiding the use of these agents . The CDC noted that there was insufficient evidence on the use of peptic ulcer prophylaxis and included no recommendations in this regard in its guidelines . The ATS/IDSA guidelines stated that the risks and benefits of prophylaxis should be weighed carefully . The most recent guidelines, developed by SHEA/IDSA, notes that histamine-2 receptor antagonists and PPIs should be avoided in patients who are not at high risk for developing a stress ulcer or stress gastritis .
There is no clear relation between prophylaxis of deep-vein thrombosis and ventilator-associated pneumonia, but the American College of Chest Physicians reported a decrease in the rate of ventilator-associated pneumonia when such prophylaxis was implemented as part of a package of interventions and included this measure in its clinical practice guidelines .
In addition to these interventions, other measures have been recommended to help prevent ventilator-associated pneumonia. One such measure is selective decontamination of the digestive tract, which involves the use of either topical antiseptic, oral antibiotics, or a brief course of systemic antibiotics . A meta-analysis (28 studies) showed that selective decontamination of the digestive or respiratory tract with use of topical antiseptic or antimicrobial agents helped reduce the frequency of ventilator-associated pneumonia in the ICU . The estimate of efficacy in prevention was 27% for antiseptics and 36% for antibiotics. Neither had an effect on mortality. This intervention is recommended in the SHEA/IDSA guidelines .
Other preventive measures are targeted primarily to the care and use of ventilator equipment and practices in direct patient care. Meticulous attention to aseptic care of the equipment is necessary, and all reusable components, such as nebulizers, should be disinfected or sterilized. Tubing circuits should be replaced after more than 48 hours, or earlier if there are signs of malfunction or contamination . Changes in the design of the endotracheal tube have also been evaluated; for example, a tube with a suction port above the cuff allows for continuous aspiration of subglottic secretions. Use of this specially designed endotracheal tube has led to significantly lower rates of ventilator-associated pneumonia, as well as shorter durations of ventilation and shorter stays in the ICU [205,206]. Among patients who had major cardiac surgery, the greatest benefit was found for patients who received ventilation for more than 48 hours . The cost of the tube is higher than traditional tubes but is offset by overall cost savings in preventing ventilator-associated pneumonia . In one meta-analysis, subglottic secretion drainage was significantly associated with a decreased incidence of ventilator-associated pneumonia, shorter time on mechanical ventilation, and longer time to the development of ventilator-associated pneumonia . The CDC, the ATS/IDSA, and the SHEA/IDSA guidelines recommend subglottic secretion drainage with this tube when possible [17,24,35].
The use of noninvasive ventilation is another measure that has reduced the incidence of ventilator-associated pneumonia [24,208,209]. In one study, the incidence decreased from 20% to 8% when noninvasive ventilation was used routinely for critically ill patients with acute exacerbation of chronic obstructive pulmonary disease or severe cardiogenic pulmonary edema . Again, the CDC, the ATS/IDSA, and the SHEA/IDSA guidelines recommend the use of noninvasive ventilation when possible [17,24,35].
The difficulty in diagnosing hospital-acquired or ventilator-associated pneumonia has been well established [17,190,211]. The clinical signs can resemble those of other, noninfectious conditions, and the specificity of clinical criteria is low . According to the CDC definition, the diagnosis in adults is made on the basis of clinical signs and symptoms and results of laboratory testing or imaging and must meet one of two criteria .
For any patient, at least one of the following:
Fever (>38°C or >100.4°F)
Leukopenia (<4000 WBC/mm3) or leukocytosis (≥12,000 WBC/mm3)
For adults ≥70 years of age, altered mental status with no other recognized cause
AND at least two of the following:
New onset of purulent sputum, or change in character of sputum, or increased respiratory secretions, or increased suctioning requirements
New onset or worsening cough, or dyspnea, or tachypnea
Rales or bronchial breath sounds
Worsening gas exchange (e.g., oxygen desaturations [e.g., PaO2/FiO2 ≤240 mm Hg], increased oxygen requirements, or increased ventilator demand)
Two or more serial chest radiographs showing at least one of the following:
New or progressive and persistent infiltrate
Pneumatoceles, in infants 1 year of age or younger
In patients without underlying pulmonary or cardiac disease (e.g., respiratory distress syndrome, pulmonary edema, chronic obstructive pulmonary disease), one definitive chest radiograph is acceptable.
There are no compelling data to recommend a specific approach to diagnosing hospital-acquired or ventilator-associated pneumonia. For patients who are not receiving mechanical ventilation, collection of a sputum specimen should be attempted before antibiotic therapy is begun [193,213]. Specimens for culture can be obtained by bronchoscopy with a protected specimen brush to limit contamination or by bronchoalveolar lavage. The latter method has been found to lead to higher rates of treatment than that based on the CDC definition, and one study showed that preferential sampling of the right lung improved the diagnostic accuracy of bronchoalvolar lavage [193,214,215]. However, the invasive procedure has disadvantages, including high cost, need for technical expertise, and potential for false-negative results [193,214]. The ATS/IDSA guidelines recommend collecting specimens from the lower respiratory tract for culture, noting that the specimens can be obtained by bronchoscopy or another means and that cultures can be quantitative or semiquantitative . A 2012 meta-analysis found no evidence that the use of quantitative cultures of respiratory secretions resulted in decreased mortality, reduced time in ICU and on mechanical ventilation, or higher rates of antibiotic change compared with qualitative cultures in patients with ventilator-associated pneumonia . In addition, mortality did not differ between invasive or noninvasive methods of obtaining samples. A 2014 follow-up study confirmed these findings .
Treatment is complicated by two divergent needs: the need for empiric therapy with a broad-spectrum antibiotic, to aid in reducing mortality rates, and the need to avoid the indiscriminate use of antibiotics, to avoid the development of resistance. To address this complex issue, the strategy of de-escalation therapy was developed. With this treatment approach, a broad-spectrum antibiotic targeted to likely pathogens is administered, and the antibiotic regimen is altered, if necessary, after the results of cultures are known [218,219]. This strategy has reduced the mortality rate while achieving an overall objective of a more judicious use of antibiotics [218,220,221]. In one study, de-escalation therapy led to a significantly lower mortality rate compared with either escalation therapy or therapy that was neither escalated nor de-escalated (17% compared with 43% and 24%, respectively) . However, de-escalation therapy was used for only 22% of the patients.
It has been emphasized that this approach, and empiric treatment of healthcare-acquired pneumonia in general, calls for knowledge of the infection history of the healthcare facility and of individual patient units [185,193,222]. Microbiology laboratory reports can provide such details, and physicians should prescribe initial antibiotics that are likely to be active against these pathogens.
The ATS/IDSA guidelines provide several recommendations for the treatment of both hospital-acquired and ventilator-associated pneumonia :
Obtain a specimen from the lower respiratory tract for culture before beginning antibiotic therapy. Do not delay initiation of therapy for critically ill patients in order to obtain specimen.
Prescribe early, appropriate, broad-spectrum antibiotic therapy with adequate doses.
Choose an empiric therapy regimen that includes agents from a different antibiotic class than what the patient has recently received.
Consider de-escalation of antibiotics after data are available on the results of cultures of specimens from lower respiratory tract cultures and the clinical response.
Use a shorter duration of antibiotic therapy (7 to 8 days) for patients with uncomplicated ventilator-associated pneumonia who have received appropriate therapy initially, have had a good clinical response, and who have no evidence of infection with nonfermenting gram-negative bacilli.
Specific treatment depends on the timing of onset and the presence or absence of risk factors for infection with multidrug-resistant organisms. For early-onset pneumonia and/or patients with no such risk factors, limited-spectrum antibiotic therapy is recommended (Table 11) . For late-onset pneumonia and/or patients at increased risk for multidrug-resistant bacteria, a broad-spectrum antibiotic therapy is recommended.
RECOMMENDED ANTIBIOTIC THERAPY FOR HEALTHCARE-ASSOCIATED PNEUMONIA ACCORDING TO SITE OF CARE
|Site of Care||Recommended Regimen|
|General ward||Antipseudomonal cephalosporin, antipseudomonal carbapenem, or extended-spectrum ß-lactam/ß-lactamase inhibitor and antipseudomonal fluoroquinolone or aminoglycoside and anti-MRSA agent (vancomycin or linezolid)|
|Intensive care unit||Empiric MRSA and double coverage of Pseudomonas pneumonia|
Vancomycin has been considered the first choice for treatment of MRSA infections . However, the ATS/IDSA guidelines note that linezolid may have advantages over vancomycin for ventilator-associated pneumonia caused by MRSA . Linezolid has been compared with vancomycin for the treatment of pneumonia caused by MRSA in many studies and has been found to improve survival and to be more cost-effective [223,224,225,226]. In one study, the rate of early microbiologic cure was not significantly higher for linezolid than for vancomycin, although there were trends favoring linezolid in several secondary clinical outcomes, such as clinical cure; duration of ventilation, hospitalization, and stay in ICU; survival time not on a ventilator; and overall survival . The findings led the authors to suggest that the benefit of linezolid may be related to factors other than bacterial clearance. The use of inhalational (aerosolized) antibiotics, alone or in combination with systemic antibiotic therapy, has proven useful for the management of highly resistant gram-negative bacillary pneumonia .
According to a meta-analysis, a short fixed-course (7 or 8 days) of antibiotic therapy may be more appropriate than a prolonged course (10 to 15 days) for patients with ventilator-associated pneumonia not caused by nonfermenting gram-negative bacilli . The short course reduced recurrence of ventilator-associated pneumonia caused by multiresistant organisms without adversely affecting other outcomes. Among patients with nonfermenting gram-negative bacilli, recurrence was greater after the short course. The authors confirmed these findings in a follow-up study published in 2015 .
Adherence to guidelines for the prevention of ventilator-associated pneumonia is low, with surveys of nurses demonstrating rates of adherence to specific preventive measures ranging from 15% to 50% [187,230]. Adherence to a bundle of prevention strategies (head-of-bed elevation, oral chlorhexidine gel, sedation holds, and a weaning protocol), with 70% compliance, led to a significant reduction in ventilator-associated pneumonia, from 32 cases per 1,000 ventilator-days to 12 cases per 1,000 ventilator-days . The IHI how-to guide on preventing ventilator-associated pneumonia provides several practical recommendations, and posting compliance with the ventilator bundle in a prominent place in the ICU can encourage and motivate staff (Table 12) .
PRACTICAL STEPS IN FOLLOWING GUIDELINES TO PREVENT VENTILATOR-ASSOCIATED PNEUMONIA
|Elevation of the Head of the Bed|
|Include the intervention on nursing flow sheets and discuss at multidisciplinary rounds. Encourage respiratory therapy staff to notify nursing staff if the head of the bed is not elevated or empower respiratory therapy staff to place the bed in this position with help of nursing staff. Include the intervention on order sets for initiation and weaning of mechanical ventilation, delivery of tube feedings, and provision of oral care.|
|Sedative Interruptions and Assessment of Readiness to Extubate|
|Implement a protocol to lighten sedation daily at an appropriate time to assess for neurologic readiness to extubate. Include precautions to prevent self-extubation, such as monitoring and vigilance, during the trial. Include a sedative interruption strategy in the overall plan to wean the patient from the ventilator; add the strategy to the weaning protocol, if available. Assess compliance each day on multidisciplinary rounds. Consider implementation of a sedation scale, such as the Richmond Agitation Sedation Scale (RASS) scale, to avoid oversedation.|
|Prophylaxis of Peptic Ulcer Disease|
|Include intervention as part of the intensive care unit admission order set and ventilation order set. Make application of prophylaxis the default value on the form. Include intervention as an item for discussion on daily multidisciplinary rounds. Empower pharmacy staff to review orders for patients in the intensive care unit to ensure that some form of prophylaxis is in place at all times for patients.|
|Prophylaxis of Deep Venous Thrombosis|
|Include intervention as part of the intensive care unit admission order set and ventilation order set. Make application of prophylaxis the default value on the form. Include intervention as an item for discussion on daily multidisciplinary rounds. Empower pharmacy staff to review orders for patients in the intensive care unit to ensure that some form of prophylaxis is in place at all times for patients.|
The use of physician-led multidisciplinary rounds with team decision making, checklists, and a focus on the ventilator bundle has led to significant reductions in ventilator-associated pneumonia [232,233,234]. Moderate strength evidence has shown that the use of audit and feedback and reminder systems improve adherence to an overall ventilator-associated pneumonia bundle as well as reduce infection rates . Education sessions have also led to enhanced knowledge and practice among healthcare professionals caring for intubated patients .
The lack of adherence to guideline-directed treatment of pneumonia cases associated with healthcare facilities is evidenced by wide variations in practice. For example, one study showed that more than 100 different antibiotic regimens had been prescribed as initial treatment and that de-escalation therapy was used for only 22% of patients . Adherence rates for treatment of pneumonia associated with healthcare facilities have been reported to be lower than rates of adherence to guidelines for treatment of community-acquired pneumonia. In one survey, guideline-recommended antibiotics were used 9% of the time for healthcare-associated pneumonia compared with 78% of the time for community-associated pneumonia . This lack of adherence was not due to unfamiliarity or disagreement with the guidelines; 71% of the survey respondents said they were aware of the guidelines, and 79% said they agreed with and practiced according to them. It is reasonable to expect that strategies used to enhance adherence to guidelines in the community-acquired pneumonia setting would also be effective in the setting of hospital-acquired and ventilator-associated pneumonia. Such strategies include feedback on performance, reminder systems, standardized order sets, and education emphasizing outcomes and cost-effectiveness.
Bloodstream infections, such as septicemia and bacteremia, can develop from other types of HAIs or infections at other sites in the body, but about half are caused by intravascular devices, primarily central venous catheters . It has been estimated that 5.3 infections occur per 1,000 catheter-days in the ICU [27,39,237]. The number of infections reported to NHSN has increased substantially, with 27,766 reported in 2009–2010, compared with 18,651 reported in 2007–2008 . These infections are also the most costly, with a mean cost of more than $50,000 per infection .
There are several types of intravascular catheters, and the risk of intravascular device-related bloodstream infections varies according to type. These catheters include:
Peripheral venous catheters
Peripheral arterial catheters
Nontunneled central venous catheters
Pulmonary artery catheters
Pressure monitoring system catheters
Peripherally inserted central venous catheters
Tunneled central venous catheters
Totally implantable devices
The nontunneled central venous catheter accounts for the majority of all intravascular device-related bloodstream infections . Peripheral catheters (arterial and venous) are rarely associated with bloodstream infections, and totally implantable catheters are associated with the lowest risk . A systematic review of 200 prospective studies of intravascular device-related bloodstream infections indicated that the level of risk associated with various types of devices can vary substantially depending on whether risk is expressed as the number of infections per 100 intravascular device-days or 1,000 intravascular device-days . The risks associated with peripheral intravenous catheters were much higher when expressed over 1,000 intravascular device-days, pointing to the need for prevention strategies targeted to all types of devices .
Other risk factors are the length of time the catheter is in place and factors related to the patient's health status (severity of illness, presence of burns or surgical wounds, compromised immune system, nutritional status) .
Intravascular device-related bloodstream infections are transmitted by both endogenous and exogenous routes. The most common cause of infection related to short-term catheters is migration of skin organisms at the site of insertion, with the organisms traveling along the surface of the catheter and colonization at the catheter tip . Direct contamination of the catheter or catheter hub by contact with hands or contaminated fluids or devices is another cause . Hematogenous seeding from another focus of infection is a less common cause, and contamination of infusion fluid is rare .
The most commonly reported pathogens for intravascular device-related bloodstream infections in 2009–2010 were coagulase-negative staphylococci (21%), S. aureus (12%), E. faecalis (9%), Candida spp. (other than C. albicans) (8%), K. pneumonia/oxytoca (8%), E. faecium (7%), and C. albicans (7%) .
The percentage of resistant S. aureus was stable compared with previous data, with a rate of 55% in 2009–2010 . Among the drug-resistant pathogens with the greatest increases compared with data for 2007–2008 were multidrug-resistant E. coli (4% vs. 2%), extended spectrum cephalosporin-resistant E. coli (19% vs. 12%), aminoglycoside-resistant P. aeruginosa (10% vs 7%), and carbapenems-resistant A. baumannii (62% vs. 50%) .
The CDC guidelines on the prevention of intravascular device-related bloodstream infections were published in 2002 and updated in 2011 . The most recent guidelines emphasize the following points :
Using maximal sterile barrier precautions during central venous catheter insertion
Using a >0.5% chlorhexidine skin preparation with alcohol for antisepsis
Avoiding routine replacement of central venous catheters as a strategy to prevent infection
Using antiseptic/antibiotic impregnated short-term central venous catheters and chlorhexidine-impregnated sponge dressings if the rate of infection is not decreasing despite adherence to other strategies
Educating and training healthcare providers who insert and maintain catheters
The CDC guidelines define maximal sterile barrier precautions as the use of a cap, mask, sterile gloves, sterile gown, and a sterile full-body drape during insertion of an intravascular device (level IB) . A sterile sleeve should also be used to protect pulmonary artery catheters during insertion (level IB) .
The CDC guidelines recommend use of an antiseptic of 70% alcohol, tincture of iodine, or chlorhexidine gluconate solution with alcohol before insertion of peripheral venous catheters (level IB) and a >0.5% chlorhexidine preparation with alcohol before insertion of central venous catheters or peripheral artery catheters and during dressing changes (category IA) . The guidelines note that chlorhexidine preparations with alcohol have not been compared with povidone iodine in alcohol and thus no recommendation can be made in this regard . In a meta-analysis of eight studies (4,143 catheters, primarily central line catheters), the chlorhexidine solution was found to reduce the risk for bloodstream infection by 49% . In a subsequent study, use of this solution led to a 1.6% decrease in the rate of bloodstream infection, a 0.23% decrease in the incidence of death, and a cost savings of $113 per catheter used compared with povidone-iodine solutions .
Most intravascular device-related bloodstream infections develop at the site of insertion, due to the density of skin flora . Rates of infection vary according to insertion site, with catheters in the internal jugular vein being associated with a greater risk of infection than catheters in the subclavian vein [27,242,243]. A 2005 study indicated that the site of insertion was not a risk factor for infection when experienced or trained healthcare workers inserted the catheters . However, such experience will not always be the norm, and the subclavian vein has been recommended by the CDC as the preferred site when possible .
Another strategy to prevent infection has been the development of central venous catheters with antimicrobial coatings. These coatings have included a combination of chlorhexidine and silver sulfadiazine and a combination of minocycline and rifampin . Both types of catheters are associated with a significantly lower rate of infection than that associated with standard catheters. When compared with each other, catheters impregnated with minocycline and rifampin were 12 times less likely to cause bloodstream infections than those coated with chlorhexidine and silver sulfadiazine . The chlorhexidine-silver sulfadiazine coating has since been enhanced, and these second-generation catheters have significantly reduced bacterial colonization, with a trend toward fewer bloodstream infections . Each coating adds to the cost of the catheter, and cost-effective analyses are necessary.
On the basis of studies of intravascular device-related bloodstream infections, a bundle consisting of five preventive measures has been recommended:
Compliance with appropriate hand hygiene
Use of maximal barrier precautions
Use of 2% chlorhexidine solution for skin antisepsis
Selection of optimal site for the catheter, with the subclavian vein as the preferred site for nontunneled catheters
Daily review of the need for the line, with prompt removal if line is deemed unnecessary
As defined by the CDC, bloodstream infections fall into two categories: laboratory-confirmed infection and clinical sepsis. Clinical sepsis is no longer used in reporting on adults and children and is restricted to use for neonates and infants . For a diagnosis of laboratory-confirmed bloodstream infection, one of the two following criteria must be met .
Recognized pathogen found on one or more blood cultures and organism cultured from blood is not related to an infection at another site
At least one of the following signs or symptoms:
Fever (>38 degrees Centigrade)
Chills (with no other recognized cause)
Hypotension (with no other recognized cause)
and signs and symptoms and positive laboratory results are not related to an infection at another site and common skin contaminant (e.g., diphtheroids, Bacillus species, Propionibacterium species, coagulase-negative staphylococci, viridans group streptococcus, Aerococcus species, or Micrococcus species) is cultured from two or more blood cultures drawn on separate occasions. Criterion elements must occur within a timeframe that does not exceed a gap of one calendar day .
There are several approaches to diagnosing an intravascular device-related bloodstream infection. A meta-analysis of 51 studies published between 1966 and 2004 was designed to identify which method was the most accurate . The studies had involved the eight most commonly used diagnostic methods: culture (qualitative, semiquantitative, or quantitative) of a catheter segment; culture (qualitative or quantitative) of blood obtained through the catheter; paired quantitative cultures (blood obtained through the catheter as well as from a peripheral site); differential time to positivity (monitoring of cultures of blood obtained through the catheter and from a peripheral site); and acridine orange leukocyte cytospin. The paired cultures method was the most accurate, with a pooled specificity of 99%, followed by qualitative culture of blood drawn through the catheter and acridine orange leukocyte cytospin .
Treatment of an intravascular device-related bloodstream infection does not always include removal of the device. Authors of consensus-based treatment guidelines advise that the decision to remove a tunneled catheter or implanted device suspected to be the source of bacteremia or fungemia should be based on the following factors :
Underlying health status of the patient
Type of catheter
Strength of the evidence that the catheter is the source of the infection
Presence of local or systemic complications
Nontunneled central venous catheters should be removed in most cases of bacteremia or fungemia . Antibiotic therapy alone has resolved 80% of infections caused by coagulase-negative staphylococcal bacteria, but in cases of infection with S. aureus or Candida, infection has persisted when the catheter has been maintained [249,250].
One strategy was developed in an attempt to retain the catheter. With so-called antibiotic lock therapy, antibiotics are instilled through the catheter after injection of an anticoagulant, locking a high concentration of the antibiotic in the lumen . This approach is used in combination with systemic antibiotic therapy, and the antibiotics used have included vancomycin, cefazolin, and clindamycin. Fluconazole and amphotericin B have been used occasionally for infection with Candida spp., and another flush solution (low concentrations of minocycline and EDTA) has demonstrated activity against staphylococci, gram-negative bacilli, and Candida spp. . Early empiric antifungal therapy is important if infection with Candida is suspected, as delayed treatment has been associated with higher mortality .
The guidelines for management of intravascular device-related bloodstream infection suggest antimicrobial treatment according to the pathogen (Table 13) . Empiric antibiotic therapy should be selected according to likely pathogens, with vancomycin recommended as initial treatment for coagulase-negative staphylococci; this treatment should be changed to semisynthetic penicillin if the identified pathogen is sensitive . Vancomycin should not be used as a front-line treatment for infections with S. aureus.
TREATMENT OF INTRAVASCULAR DEVICE-RELATED BLOODSTREAM INFECTIONS IN ADULTS
|Pathogen||Preferred Antimicrobial Agent|
Enterobacter spp. and Serratia marcescens
|Escherichia coli and Klebsiella spp.||Third-generation cephalosporin|
|Enterobacter spp. and Serratia marcescens||Carbapenem|
|Acinetobacter baumannii||Ampicillin/sulbactam or carbapenem|
|Pseudomonas aeruginosa||Fourth-generation cephalosporin or carbapenem or antipseudomonal beta-lactam plus aminoglycoside|
|Burkholderia cepacia||SMZ-TMP or carbapenem|
|Candida albicans or Candida spp.||Echinocandin or fluconazole|
|Mycobacterium spp.||Susceptibility varies by species|
If fever or other signs of infection persist after removal of the catheter, the patient should be evaluated for other infection, especially endocarditis. Bacterial endocarditis has been found in 25% of patients with intravascular device-related bloodstream infection caused by S. aureus . The findings of one study suggested that patients with MRSA bacteremia and underlying chronic liver disease were at higher risk for endocarditis . Transesophageal echocardiogram can aid in determining the presence of this infection.
As is the case with guidelines for other HAIs, adherence to prevention guidelines is suboptimal. A survey of more than 500 hospitals showed that, while adherence to the two most strongly recommended prevention strategies—maximal sterile barrier precautions and antisepsis with chlorhexidine gluconate—was good at VA hospitals (84% and 91%, respectively), the rates were lower at non-VA hospitals (71% and 69%) . Adherence to a combination of maximal sterile barrier precautions, chlorhexidine gluconate, and avoidance of central line changes was even lower: 62% and 44%, respectively . In another study, central venous catheters were routinely changed to prevent infection in about 15% of hospitals .
Implementing a prevention bundle has significantly reduced intravascular device-related bloodstream infections: the decrease was from 5.9 per 1,000 catheter-days to 3.1 per 1,000 in one study and from 7.7 per 1,000 catheter-days to 1.4 per 1,000 in another [56,232]. A how-to guide developed by the IHI provides practical suggestions for implementing the bundle (Table 14) . A checklist should be developed for use when inserting a catheter to ensure adherence to all prevention strategies .
PRACTICAL STEPS IN FOLLOWING GUIDELINES TO PREVENT INTRAVASCULAR DEVICE-RELATED BLOODSTREAM INFECTIONS
|Include hand hygiene as part of the checklist for placement of central lines. Keep soap/alcohol-based hand hygiene dispensers prominently placed, and make universal precautions equipment, such as gloves, available only near hand sanitation equipment. Post reminder signs at the entry and exits to patient rooms. Initiate a campaign using posters including photos of celebrated hospital physicians/employees recommending hand hygiene. Create an environment in which reminding each other about hand hygiene is encouraged.|
|Maximal Barrier Precautions|
|Include maximal barrier precautions as part of the checklist for placement of central lines. Keep equipment stocked in a cart for central line placement to avoid the difficulty of finding necessary equipment to institute maximal barrier precautions. If a full-size drape is not available, apply two drapes to cover the patient or consult with the operating room staff to determine how to obtain full-size sterile drapes, as they are used routinely in surgical settings.|
|Chlorhexidine Skin Antisepsis|
|Include chlorhexidine antisepsis as part of the checklist for placement of central lines. Include chlorhexidine antisepsis kits in carts or grab bags storing central line equipment. (Many prepared central line kits include povidone-iodine kits, and these must be avoided.) Ensure that the solution dries completely before attempting to insert the central line.|
|Selection of Optimal Insertion Site|
|Include optimal site selection as part of the checklist for placement of central lines, with room to note appropriate contraindications (e.g., bleeding risks).|
|Daily Review of Need for Central Line|
|Include daily review of the need for the central line as part of multidisciplinary rounds. Include assessment for removal of central lines as part of daily goal sheets. Record time and date of line placement for record-keeping purposes and evaluation by staff to aid in decision making.|
Adherence to appropriate postinsertion care has been the focus of some studies. In one study, there were breaches in postinsertion care in 45% of cases . The primary breaches were non-intact dressing (158 breaches per 1,000 catheter-days) and incorrectly placed caps and taps (156 breaches per 1,000 catheter-days) . The rate of intravascular device-related bloodstream infection during the study period was 5.5 per 1,000 catheter-days . In another study, nursing staff used a postinsertion care bundle that consisted of the following: daily inspection of the insertion site; site care if the dressing was wet, soiled, or had not been changed for 7 days; documentation of ongoing need for the catheter; proper application of a chlorhexidine gluconate-impregnated sponge at the insertion site; appropriate hand hygiene before handling the intravenous system; and application of an alcohol scrub to the infusion hub for 15 seconds before each entry . Adherence to this bundle led to a significant decrease in intravascular device-related bloodstream infections, from 5.7 per 1,000 catheter-days to 1.1 per 1,000 catheter-days .
The availability of policies regarding prevention strategies is also lacking. Although 80% of 25 ICUs (10 hospitals) had written policies for insertion of central venous catheters, only 28% had a policy requiring maximal sterile barrier precautions, and 36% and 60% of the units required hand hygiene before accessing a central venous catheter or treating the exit site, respectively . A formal educational program on catheter insertion was in place at 52% of the units . Education, in the form of self-study modules with pretest and post-test, along with didactic lectures and integration of evidence-based guidelines have been associated with increases in adherence to recommended practices and decreases in bloodstream infections .
A systematic review demonstrated moderate strength of evidence for audit and feedback and provider reminder systems, along with base strategies .
C. difficile is the most common cause of infectious diarrhea among adults in healthcare settings . Colonization with the inactive spore is much more prevalent in the healthcare setting than in the community, with a rate of approximately 2% to 3% in the community compared with 50% in the healthcare setting . Although only colonization with C. difficile occurs commonly, usually the production of toxins (A and B) leads to inflammation, secretion of mucous and fluid, and damage to the mucosa, resulting in diarrhea or colitis . Disease can further progress to toxic megacolon, sepsis with or without intestinal perforation, and death [260,261].
C. difficile has reached an epidemic level; the incidence more than tripled between the 1990s and 2005 (from 30 to 40 cases per 100,000 individuals to 131 per 100,000) . During this same time, some bacterial strains have become more virulent and perhaps more resistant . The greatest increase in incidence is among people 65 years of age or older, with rates more than fivefold higher than those among people 45 to 64 years of age . As with other HAIs, C. difficile infection in the healthcare setting has been associated with increased length of stays, increased mortality, and higher costs [129,264,265,266,267].
The primary risk factors for infection with C. difficile are antibiotic use, older age, and hospitalization . Antibiotic use was reported as the cause in more than 96% of hospitalized patients in one study . Fluoroquinolones is one of the primary classes of antibiotics associated with C. difficile, but virtually every antibiotic has been associated with the infection . The risk of infection increases with longer hospitalizations, with a 15% to 45% risk of colonization among patients hospitalized for 1 to 3 weeks .
C. difficile is an exogenous infection that is transmitted through the fecal-oral route. The pathogen can also spread through contact with surfaces (commodes, bath tubs), devices (rectal thermometers), or materials that are contaminated with feces.
Guidelines developed by SHEA/IDSA offer several recommendations for prevention and control of C. difficile, categorized as restriction of antibiotic use; measures for healthcare workers, patients, and visitors; and environmental cleaning and disinfection (Table 15) . The guidelines note that the use of antibiotics should be minimized and that an antibiotic stewardship should be implemented . Appropriate hand hygiene is essential, and soap and water should be used rather than alcohol-based handrubs, as alcohol is not effective at killing C. difficile spores . Gowns, gloves, and contact precautions for the duration of diarrhea are also recommended. The guidelines suggest that removing environmental sources of C. difficile, such as replacing rectal thermometers with disposable ones, can help reduce the incidence of C. difficile infection. The guidelines also note that the following are not recommended: routine environmental screening for C. difficile (level III, C); routine identification of asymptomatic carriers for infection control purposes (level III, A); and use of probiotics to prevent infection (level I, B) .
SHEA/IDSA GUIDELINES FOR INFECTION CONTROL MEASURES FOR CLOSTRIDIUM DIFFICILE
Restriction of Antibiotic Use
Measures for Healthcare Workers, Patients, and Visitors
Environmental Cleaning and Disinfection
Infection with C. difficile is diagnosed on the basis of clinical findings and the results of laboratory testing . C. difficile infection is defined as (1) the presence of diarrhea (passage of three or more unformed stools in up to 24 consecutive hours) and (2) positive results on stool testing for the presence of toxigenic C. difficile or its toxins or findings of pseudomembranous colitis on colonoscopy or histopathologic evaluation . Diarrhea may be absent in up to 20% of patients with fulminant colitis or postoperative ileus . Other symptoms include fever, nausea, vomiting, abdominal pain or tenderness, and loss of appetite, but these symptoms are found in about half of patients with the infection [32,259].
Diagnostic stool testing should be done only on unformed stool (level II, B), and testing for asymptomatic patients is not useful (level III, B) . Repeat testing during the same episode of diarrhea is discouraged, as it does not provide clinically useful information (level II, B) .
Several diagnostic tests are available to detect C. difficile, and they vary in terms of sensitivity, specificity, and turnaround times. Stool culture is the most sensitive test, but it is not clinically practical because of the slow turnaround time . The sensitivity of cell cytotoxicity assay has been reported to range from 67% to 100%, whereas enzyme immunoassay testing for toxins A and B has a sensitivity ranging from 63% to 94% and a specificity of 75% to 100% . Enzyme immunoassay testing is rapid and less expensive than other tests but it is a suboptimal choice compared with cell cytotoxicity assay (level II, B) . The SHEA/IDSA guidelines note that polymerase chain reaction testing appears to be rapid, sensitive, and specific, but more data on its usefulness are needed before it can be recommended for routine use (level II, B) .
The most important step in treating C. difficile-associated diarrhea is to discontinue the inciting antibiotic as soon as possible . This approach alone will lead to resolution of diarrhea in approximately 15% to 25% of patients with mild infection [259,268]. Antibiotic treatment of the diarrhea should not begin until the culture results are known, as approximately 30% of hospitalized patients with antibiotic-associated diarrhea will have C. difficile infection . However, if severe or complicated C. difficile infection is suspected, empirical treatment should be started as soon as the diagnosis is suspected (level III, C) . The SHEA/IDSA guidelines recommend metronidazole or vancomycin, depending on the severity of infection (Table 16) . Subtotal colectomy with preservation of the rectum should be considered for patients who are severely ill (level II, B). Metronidazole should not be used beyond the first recurrence of C. difficile infection or for long-term treatment because of the potential for cumulative neurotoxicity . Treatment is not recommended for asymptomatic carriers (level I, B).
SHEA/IDSA GUIDELINES FOR THE TREATMENT OF CLOSTRIDIUM DIFFICILE INFECTION ACCORDING TO SEVERITY OF DISEASE
|Severity of Disease||Preferred Treatment|
|Mild to moderate||Metronidazole, PO, 500 mg, 3 times per day for 10 to 14 days (level I, A)|
|Severe||Vancomycin, PO, 125 mg, 4 times per day for 10 to 14 days (level I, B)|
|Severe, complicated||Vancomycin, PO, 500 mg, 4 times per day, with or without metronidazole, IV, 500 mg every 8 hrsa (level III, C)|
|aIf ileus is present, vancomycin may be given per rectum as a retention enema, at a dose of 500 mg/100 mL normal saline, every 6 hours.|
In addition to infection-directed antibiotics, treatment of C. difficile infection also includes fluid replacement, and electrolyte normalization . The use of antiperistaltic agents should be avoided, as they may obscure symptoms and precipitate toxic megacolon (level III, C) . The use of probiotics has been suggested as an adjunct to antibiotic treatment, but a systematic review found insufficient data to support probiotics as adjunct therapy and no evidence to support its use alone .
The development of formal infection control programs in hospitals and other healthcare facilities was spurred by the Joint Commission accreditation standards for infection control, published in 1976. According to the standards, accredited facilities must have a program for the surveillance, prevention, and control of HAIs . In 1974, the CDC designed the Study on the Efficacy of Nosocomial Infection Control project to determine if infection surveillance and infection control programs could reduce the number of HAIs . The nationwide study evaluated rates of HAIs in hospitals before and after the implementation of infection control programs; the researchers noted that programs with four components were associated with a one-third reduction in the rate of HAIs: an effective hospital epidemiologist, one infection control practitioner for every 250 beds, active surveillance mechanisms, and ongoing control efforts . With the increased focus on prevention of HAIs, infection control professionals have come to be known as infection preventionists .
An infection control program is usually overseen by a committee chaired by an infectious disease physician and consisting of staff representing departments throughout the facility, such as nursing, pharmacy, surgery, clinical microbiology, central sterilization services, housekeeping, maintenance, food services, and laundry services. Among the responsibilities of an infection control program are to:
Conduct surveillance of HAIs
Develop policies regarding prevention and control, such as hand hygiene and precautions
Ensure adherence to standards for environmental services
Establish a program to monitor and evaluate antimicrobial therapy
Provide education to healthcare workers about adherence to infection control policies
Develop guidelines for outbreak preparedness
The policies and procedures in each of these areas, as well as guidelines for adherence, should be documented in an infection control manual.
All physicians and staff within a healthcare facility have responsibility for helping to advance infection control goals. Physicians should assume the following responsibilities :
Protect their patients from other infected patients or staff
Comply with the practices approved by the infection control committee
Obtain appropriate microbiologic specimens when infection is suspected or present
Notify the infection control committee about confirmed cases of HAIs
Comply with the institution's recommendations regarding the use of antibiotics
Educate patients, visitors, and staff about techniques to prevent the transmission of infection.
As direct providers of care in a healthcare facility, the nursing staff plays a substantial role in carrying out infection control practices. Nursing administrators should promote the development and enhancement of nursing techniques, review nursing policies regarding aseptic techniques, and offer educational training programs on best practices . Nurses on patient care units have the following responsibilities :
Comply with established infection control practices
Monitor aseptic techniques, including handwashing and use of isolation precautions
Report evidence of infection immediately to the attending physician
Initiate patient isolation and order culture specimens when infection is suspected and a physician is not immediately available
Limit patient exposure to infections from others (visitors, hospital staff, other patients, or equipment used for diagnosis or treatment)
Community hospitals have had success with participating in an infection control network. In 12 community hospitals in North Carolina and Virginia that joined such a network (the Duke Infection Control Outreach Network), there were significant decreases in the annual rates of healthcare-associated bloodstream infections, infection and colonization with MRSA, ventilator-associated pneumonia, and exposure of staff to bloodborne pathogens . After network participation for 5 years, the average decrease in the number of device-related infections and HAIs due to MRSA decreased by an average of 50% . The cost savings was approximately $100,000 per hospital, and in total, an estimated 52 to 105 deaths related to ventilator-associated pneumonia or intravascular device-related infection were prevented .
Most prevention and control policies focus on general measures, such as surveillance; adherence to guidelines for hand hygiene, influenza vaccination, precautions and isolation techniques, management of drug-resistant micro-organisms, and standards for environmental services; and education of healthcare workers as well as patients and families.
Surveillance is an essential component of an infection control program. The infection control team has traditionally conducted surveillance through open communication with the nursing staff and physicians and meticulous review of patient records and microbiology results. The infections most commonly targeted for surveillance are those associated with substantial costs in terms of morbidity, mortality, or economics, and those difficult to treat. In addition, infections with a predilection for epidemics are a focus. The data gathered should be evaluated in relation to regional and national norms, and temporal trends should also be noted. Continuing analysis of the data allows the infection control team to evaluate the efficacy of programs designed to enhance compliance with hospital-wide strategies to prevent HAIs.
Hand hygiene is the most important preventive measure in hospitals, and the Joint Commission mandates that hospitals and other healthcare facilities comply with the Level I recommendations in the CDC guidelines for hand hygiene . The CDC guidelines state the specific indications for washing hands, the recommended hand hygiene techniques, and recommendations about fingernails and the use of gloves (Table 17) . The guidelines also provide recommendations for surgical hand antisepsis, selection of hand-hygiene agents, skin care, educational and motivational programs for healthcare workers, and administrative measures.
SUMMARY OF CDC RECOMMENDATIONS FOR HAND HYGIENE
|Indications for Hand Hygiene|
|Wash hands with nonantimicrobial or antimicrobial soap and water when they are visibly dirty, contaminated, or soiled. If hands are not visibly soiled, use an alcohol-based handrub for routinely decontaminating hands.|
|Recommended Handrub Technique|
|Apply to palm of one hand, rub hands together, covering all surfaces until dry.|
|Recommended Handwashing Techniques|
|Fingernails and Artificial Nails|
|Keep tips of natural nails to a length of ¼ inch. Do not wear artificial nails during direct contact with high-risk patients (e.g., patients in intensive care unit or operating room).|
|Use of Gloves|
|Use gloves when there is potential for contact with blood or other potentially infectious materials, mucous membranes, or nonintact skin. Change gloves after use for each patient.|
Despite the simplicity of the intervention, its substantial impact, and wide dissemination of the guidelines, compliance with recommended hand hygiene has ranged from 16% to 81%, with an average of 30% to 50% [26,39,40,41,42] A 2010 systematic review of studies on compliance with hand-hygiene guidelines in hospital care found an overall median compliance rate of 40%, with lower rates in intensive care units (30% to 40%) than in other settings (50% to 60%), lower rates among physicians than among nurses (32% and 49%, respectively), and lower rates before (21%) rather than after (47%) patient contact . Among the reasons given for the lack of compliance are inconvenience, understaffing, and damage to skin [26,40,87]. The development of effective alcohol-based handrub solutions addresses these concerns, and studies have demonstrated that these solutions, as well as performance feedback and accessibility of materials, have increased compliance [41,276,277,278]. The CDC guidelines recommend the use of handrub solutions on the basis of several advantages, including :
Better efficacy against both gram-negative and gram-positive bacteria, mycobacteria, fungi, and viruses than either soap and water or antimicrobial soaps (such as chlorhexidine)
More rapid disinfection than other hand-hygiene techniques
Less damaging to skin
Time savings (18 minutes compared with 56 minutes per 8-hour shift)
The guidelines suggest that healthcare facilities promote compliance by making the handrub solution available in dispensers in convenient locations (such as the entrance to patients' room or at the bedside) and provide individual pocket-sized containers . The handrub solution may be used in all clinical situations except for when hands are visibly dirty or are contaminated with blood or body fluids. In such instances, soap (either antimicrobial or nonantimicrobial) and water must be used.
However, there are many other reasons for lack of adherence to appropriate hand hygiene, including denial about risks, forgetfulness, and belief that gloves provide sufficient protection [26,40]. These reasons demand education for healthcare professionals to emphasize the importance of hand hygiene. Also necessary is research to determine which interventions are most likely to improve hand-hygiene practices, as no studies have demonstrated the superiority of any intervention . Single interventions are unlikely to be effective .
Several single-institution studies have demonstrated that appropriate hand hygiene reduces overall rates of HAIs, including those caused by MRSA and VRE [42,277,278]. However, rigorous evidence linking hand hygiene alone with the prevention of HAIs is lacking, making it difficult to evaluate the true impact of hand hygiene alone in reducing HAIs . One challenge in evaluating the impact of hand hygiene is that a variety of methodologies have been used to assess compliance (surveys, direct observation, measurement of product use), each with its own advantages and disadvantages . Measuring the effect of appropriate hand hygiene alone is also difficult because the intervention is often one aspect of a multicomponent strategy to reduce infection . Lastly, as noted previously, the development of HAIs is complex, with many contributing factors. Although more research is needed to assess the individual impact of appropriate hand hygiene, this basic prevention measure is the essential foundation of an effective infection control strategy and an element of every infection control guideline.
The vaccination status of healthcare workers has been found to have a direct effect on transmission of the influenza virus to patients. Outbreaks of influenza in healthcare settings have been associated with low rates of vaccination among healthcare workers, and lower rates of nosocomial influenza have been related to higher vaccination rates among healthcare workers [281,282]. Because of these findings, several organizations have addressed the need for vaccination. The Advisory Committee on Immunization Practices recommends annual influenza vaccination for all healthcare workers . CDC guidelines include four Level I recommendations to help increase rates of vaccination :
Offer influenza vaccine annually to all eligible healthcare workers.
Provide influenza vaccination to healthcare workers at the work site and at no cost as one component of employee health programs. Use strategies that have been demonstrated to increase influenza vaccine acceptance, including vaccination clinics, mobile carts, vaccination access during all work shifts, and modeling and support by institutional leaders.
Monitor influenza vaccination coverage and declination of healthcare workers at regular intervals during influenza season and provide feedback of ward-, unit-, and specialty-specific rates to staff and administration.
Educate healthcare workers about the benefits of influenza vaccination and the potential health consequences of influenza illness for themselves and their patients, the epidemiology and modes of transmission, diagnosis, treatment, and nonvaccine infection control strategies, in accordance with their level of responsibility in preventing healthcare-associated influenza.
In addition, the Joint Commission began including vaccination programs in its accreditation standards in 2007 .
Despite these guidelines, not all healthcare personnel are being vaccinated for influenza. The CDC estimates that 64.3% of healthcare personnel were vaccinated during the period November 2014 to early 2015, which was similar to early season coverage during the 2013–2014 influenza season (62.9%) . Healthcare workers have given many reasons for not being vaccinated, and the reasons vary among categories of healthcare professionals . Across all categories, shortage of the vaccine is the primary reason for not being vaccinated; other reasons include concern about side effects, inconvenience, and forgetfulness . Many reasons for receiving the vaccine have also been identified, including [286,287]:
Fear of getting influenza
Fear of transmitting influenza to patients
Belief that the vaccine is safe
Belief that the vaccine is effective
The CDC reports that vaccination rates are highest among healthcare personnel whose employers require (85.8%) or recommend (68.4%) that they be vaccinated, compared with personnel whose employers who do not recommend or have a policy recommending vaccination (43.4%) . Efforts to increase the vaccination rate among healthcare workers are ongoing. The APIC issued a position paper acknowledging the problem and highlighting suggestions to improve vaccination rates .
The CDC guidelines for isolation precautions in hospitals, updated in 2007, synthesize a variety of recommendations for precautions based on the type of infection and the route of transmission . As defined by the CDC, Standard Precautions represent measures that should be followed for all patients in a healthcare facility, regardless of diagnosis or infection status. Standard Precautions apply to blood; all body fluids, secretions, and excretions except sweat, regardless of whether or not they contain visible blood; nonintact skin; and mucous membranes . For patients who are known to have or are highly suspected to have colonization or infection, Contact Precautions should be followed. This type of precaution is designed to reduce exogenous transmission of micro-organisms through direct or indirect contact from healthcare workers or other patients. Airborne Precautions are used for patients who have or are highly suspected of having infection that is spread by airborne droplet nuclei, such as tuberculosis, measles, or varicella. Droplet Precautions target infections that are transmitted through larger droplets generated through talking, sneezing, or coughing, such as invasive Haemophilus influenzae type b disease, diphtheria (pharyngeal), pertussis, group A streptococcal pharyngitis, influenza, mumps, and rubella .
The CDC guidelines include descriptions of all the elements involved in the four types of precautions, including hand hygiene; the use of personal protection equipment (gloves, gown, and face protection); handling of patient-care equipment; environmental services and occupational health; and placement of the patient. A new element of Standard Precautions added to the 2007 guidelines is respiratory hygiene/cough etiquette . Recommendations in this area address the importance of educating healthcare workers about adherence to measures to control the transmission of respiratory pathogens, especially during seasonal outbreaks of viral respiratory tract infections. In addition, the guidelines state that efforts should be made to contain respiratory secretions in patients and other individuals who have signs and symptoms of a respiratory infection, beginning at the point of initial encounter in a healthcare setting. Signs should be posted to instruct patients and visitors with symptoms of respiratory infection to cover their mouths/noses when coughing or sneezing, to use and dispose of tissues, and to perform hand hygiene after contact with respiratory secretions. Masks should be offered to coughing patients and other individuals with symptoms, and such persons should be encouraged to maintain an ideal distance of at least 3 feet from others in common waiting areas.
The management of drug-resistant organisms is a crucial aspect of an institution's infection control program. Updated guidelines for the management of MRSA and other drug-resistant micro-organisms were published by the CDC in 2006 and the SHEA in 2014; the guidelines focus on the prevention of drug-resistant infections and the judicious use of antibiotics (antimicrobial stewardship) (Table 18) [22,30,38,72].
SUMMARY OF STRATEGIES FOR PREVENTION OF METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS AND OTHER DRUG-RESISTANT MICRO-ORGANISMS
The CDC's Get Smart for Healthcare program provides 12-step fact sheets, pocket cards, posters, and slide sets for a variety of patient populations, including hospitalized adults, individuals to have surgery, patients receiving dialysis, long-term care patients, and hospitalized children . All of the resources are available on the CDC website at http://www.cdc.gov/getsmart/healthcare.
The IHI defines five components of a program to reduce the risk of infection with drug-resistant micro-organisms :
Decontamination of the environment and equipment
Contact precautions for infected and colonized patients
Bundled interventions to prevent intravascular device-related bloodstream infections and ventilator-associated pneumonia
Universal surveillance of MRSA at hospital admission has been suggested as a measure to help prevent the transmission of this infection in the healthcare setting; however, the CDC guidelines state that the evidence on universal surveillance is limited and recommends surveillance only in specific subpopulations, defined in the context of the infection characteristics of the facility .
Since the publication of the guideline, conflicting data have been reported. In a prospective study of surgical patients at a Swiss teaching hospital, a rapid MRSA screening test at the time of hospital admission did not reduce the rate of MRSA infections . In contrast, a universal MRSA screening program at a three-hospital organization in the United States led to a large reduction in MRSA infection during hospitalization and at 30 days after discharge . Rates of MRSA infection have been reduced when universal MRSA surveillance was incorporated into a bundle of interventions that included adherence to Standard Precautions and recommendations for hand hygiene, adherence to Contact Precautions for patients who have MRSA-positive cultures, and efforts to change the environmental culture through briefings on patient care units, leadership involvement, and other similar strategies . In one study, implementation of such a bundle resulted in significant decreases in transmission of MRSA (from 5.8 per 1,000 bed-days to 3.0 per 1,000) and overall MRSA HAIs (from 2.0 per 1,000 bed-days to 1.0 per 1,000), as well as a 65% decrease in MRSA surgical site infections after orthopedic operations . Three independent factors have been found to correlate with previously unknown MRSA carriage: recent treatment with antibiotics, history of hospitalization, and age older than 75 years. Predictive models with these factors may enhance MRSA screening by better targeting patients at risk for MRSA carriage .
The principles underlying the judicious use of antibiotics are the limitation of unnecessary antibiotics, obtaining timely culture and sensitivity data, selecting the most appropriate treatment, and prescribing the appropriate dose . In addition, studies have shown that antimicrobial use can be decreased by using explicit criteria to identify patients with HAIs as well as those at highest risk for infection . In their "Guidelines for Developing an Institutional Program to Enhance Antimicrobial Stewardship," SHEA and IDSA recommend that two core strategies of such a program are a prospective audit with intervention and feedback and formulary restriction and preauthorization . Other elements of an effective antimicrobial stewardship program include :
Education to supplement interventions
Guidelines and clinical pathways that incorporate local microbiology and resistance patterns
Antimicrobial order forms
Policy to avoid routine antimicrobial cycling
Selective use of combination therapy
Streamlining or de-escalation of therapy
Systematic plan for parental-to-oral conversion
Education on best practices is a crucial aspect of preventing HAIs and is a recommendation in all infection control guidelines. Education should highlight the effect of prevention measures on the rates of HAIs, enhance knowledge about currently available guidelines, and provide instruction on carrying out guideline recommendations. Research has also suggested that education about prevention strategies may be more effective if patterns of care and levels of risk are incorporated into recommendations . Numerous studies have shown that knowledge and practices related to HAIs and guidelines are improved after educational programs. The combination of a self-study module (with pretest and post-test), inservice lectures, posters, and fact sheets on the prevention of intravascular device-related bloodstream infections and appropriate practices led to substantial reductions in the prevalence of such infections [258,296,297]. A small study showed that ICU nurses' knowledge and practices were enhanced by education on the prevention of ventilator-associated pneumonia . A Canadian study demonstrated that rates of nosocomial MRSA infection significantly decreased after a mandatory infection control education program on MRSA that included discussion of hospital-specific MRSA data and case-based practice .
Because increasing knowledge is not sufficient for effecting behavior change, theoretical models for behavior change should be considered when designing improvement initiatives [280,299]. Among effective model-related strategies are the following [280,299]:
Education and discussion of barriers to adherence (cognitive model)
External reinforcements, incentives, and reminders (behavioral model)
Consensus, leadership, and role models (social influence model)
Quality improvement teams, process redesign, and fostering of a safety- oriented culture (organizational model)
Healthcare facilities should explore innovative ways to develop quality improvement initiatives. In an effort to enhance adherence to the CDC guidelines on hand hygiene, a group of three hospitals used the Six Sigma approach with success. Six Sigma is a process established in the business world to achieve and sustain excellence in general operations and service . The healthcare facility used the process to organize the knowledge, opinions, and actions of physicians, nurses, and other staff in four ICUs at the facilities, resulting in an increase in compliance from 47% to 80% .
Given the low rates of influenza vaccination among healthcare workers, education on the importance of this measure is also needed. Two literature reviews have shown high rates of misconceptions or lack of knowledge about influenza, the role of healthcare professionals in transmitting influenza to patients, and the importance and risks of vaccination [302,303]. Education on vaccination should be targeted to address these attitudes and beliefs. In addition, some studies have indicated that self-protection is a primary reason healthcare professionals decide to be vaccinated, and education that focuses on this aspect may help improve vaccination rates .
Education for patients and families is an important component of an overall prevention strategy, and the U.S. Department of Health and Human Services notes that such education is a critical part of the national effort on preventing HAIs . Many national-level initiatives have been launched to encourage individuals to become more active in their health care and to be their own advocates, and patients, family members, and hospital visitors should be encouraged to become partners in preventing the transmission of infection in the healthcare setting .
Hospitals should engage patients in their own care by discussing infection control measures for hand hygiene practices, respiratory hygiene practices, and contact precautions (according to the patient's condition) with the patient and his or her family members on the day the patient enters the hospital or as soon as possible thereafter. For patients who are to have surgery, healthcare professionals should describe the measures that will be taken to prevent adverse events. This information may be provided in any form of media, and the patient's understanding of the information should be evaluated and documented.
Physicians and other healthcare professionals should educate patients and families about ways to prevent infection, especially with regard to their specific factors (e.g., surgery, insertion of a urinary catheter). Clinicians should also explain the importance of the appropriate use of antibiotics, including the need to complete the recommended antibiotic treatment course; the relationship between the inappropriate use of antibiotics and the increasing prevalence of drug-resistant bacteria; and the implications of drug-resistant bacteria. Patients should be encouraged to help promote adequate hand hygiene by asking their healthcare providers if they have washed their hands. The IHI has addressed this topic with the "It's OK to Ask" campaign, and patient educational pamphlets can be downloaded from the IHI website (http://www.ihi.org). The CDC has developed a video for newly admitted patients on the topic of hand hygiene, which is available on its website (http://www.cdc.gov/handhygiene/Patient_materials.html). SHEA and the CDC collaborated to develop a series of patient guides on the top five HAIs, as well as on MRSA and VRE, and the guides are available on the SHEA website (http://www.shea-online.org/Patients.aspx).
The ability to understand health information and make informed health decisions, known as health literacy, is integral to good health outcomes . Yet, the National Assessment of Adult Literacy estimated that only 12% of adults have "proficient" health literacy and 14% have "below basic" health literacy . Rates of health literacy are especially low among ethnic minority populations and individuals older than 60 years of age . Compounding the issue of health literacy is the high rate of individuals with limited English proficiency. According to the U.S. Census Bureau data from 2014, more than 61.4 million Americans speak a language other than English in the home, with more than 25 million of them (8.6% of the population) speaking English less than "very well" .
Clinicians should assess their patients' literacy level and understanding and implement interventions as appropriate. Healthcare professionals should use plain language in their discussions with patients who have low literacy or limited English proficiency. They should ask them to repeat pertinent information in their own words to confirm understanding. Reinforcement with the use of low-literacy or translated educational materials may be helpful.
Translation services should be provided for patients who do not understand the clinician's language. "Ad hoc" interpreters (family members, friends, bilingual staff members) are often used instead of professional interpreters for a variety of reasons, including convenience and cost. However, clinicians should check with their state's health officials about the use of ad hoc interpreters, as several states have laws about who can interpret medical information for a patient . Children should especially be avoided as interpreters, as their understanding of medical language is limited and they may filter information to protect their parents or other adult family members . Individuals with limited English language skills have actually indicated a preference for professional interpreters rather than family members . Most important, perhaps, is the fact that clinical consequences are more likely with ad hoc interpreters than with professional interpreters [309,310,311].
The American Medical Association offers several health literacy resources for healthcare professionals on its website (http://www.ama-assn.org), and the U.S. Department of Health and Human Services offers valuable information on cultural competency from the Health Resources and Services Administration (HRSA) (http://www.hrsa.gov/culturalcompetence) and the Office of Minority Health (http://www.thinkculturalhealth.org).
Another responsibility of an infection control team is establishing response plans for outbreaks and epidemics and controlling them should they occur. An outbreak is defined by WHO as "an unusual or unexpected increase of cases of a known nosocomial infection or the emergence of cases of a new infection" . The number of individuals affected can vary from a few to 100 or more. Outbreaks and epidemics account for approximately 5% to 10% of HAIs, and most hospitals lack adequate equipment, isolation space, and staff to treat a large increase in the number of patients with an infectious disease [39,87]. The two primary concerns are to confirm the existence of the outbreak and to establish control measures to confine the spread.
An outbreak should be identified and investigated as early as possible to prevent morbidity and mortality. Any healthcare professional who suspects an outbreak should notify infection control staff, and an outbreak team should be established. Investigating an outbreak involves [15,312]:
Establishing the existence of an outbreak
Verifying the diagnosis
Defining and identifying cases
Describing and orienting the data in terms of time, place, and person
Developing and evaluating hypotheses
Refining hypotheses and carrying out additional studies
Implementing control and prevention measures
The outbreak team should collaborate with all appropriate healthcare workers to identify either the carriers or the common sources of the infection and to review aseptic practices and disinfectant use for a breach in compliance. Data on potential cases should be reviewed and a case definition should be developed. The case definition should include [15,312]:
Unit of time and place
Specific biologic and/or clinical criteria
Gradient of definition (definite, probable, or possible)
Differentiation between colonization and infection
Specific criteria to identify the index case, if relevant information is available
Data should be collected from all available sources, such as patient charts, microbiology reports, pharmacy reports, and log books from patient units. Describing the outbreak in terms of individuals, place, and time helps to create an epidemic curve, which shows the distribution of cases by time of onset . An attack rate can then be defined as the number of people at risk who are infected compared with the total number of people at risk.
Developing and evaluating hypotheses will yield the source of the outbreak and/or the index case. The data should be reviewed carefully to evaluate the characteristics and similarities among affected individuals. The team must then determine the extent of the outbreak. Cohort isolation is implemented as needed (Table 19) [22,313]. Throughout the investigation, the team should communicate routinely with hospital administration. At completion, data on the outbreak should be documented and published, as the information can provide valuable education to the healthcare community at large and can help staff prepare for future outbreak investigations .
TYPE AND DURATION OF PRECAUTIONS REQUIRED FOR INFECTIONS WITH POTENTIAL FOR OUTBREAKS
|Infection/Condition||Precaution Type||Precaution Duration||Notes|
|Anthrax (cutaneous or pulmonary)||Standard||Ongoing||Use Contact Precautions if there is large amount of uncontained drainage from lesions.|
|Aspergillosis||Standard||Ongoing||Use Contact Precautions and Airborne Precautions if there is massive soft-tissue infection with copious drainage.|
|Botulism||Standard||Ongoing||Not transmitted person-to-person.|
|Diphtheria (cutaneous or pharyngeal)||Contact, Droplet||Until antibiotic therapy is completed and two cultures taken at least 24 hours apart are negative||—|
|Ebola (viral hemorrhagic fever)||Standard, Contact, Droplet||Duration to be determined on case-by-case basis, in conjunction with local, state, and federal health authorities||Single patient room with the door closed preferred. Maintain log of all people entering the patient's room. Use barrier protection against blood and body fluids upon entry into room (single gloves and fluid-resistant or impermeable gown, face/eye protection with masks, goggles or face shields). Use additional protective wear (double gloves, leg and shoe coverings) during final stages of illness when hemorrhage may occur. Use dedicated disposable (preferred) medical equipment for patient care. Clean/disinfect all nondedicated, nondisposable equipment. Limit use of needles, sharps as much as possible. Limit procedures, tests. Avoid aerosol-generating procedures. Notify public health officials immediately if Ebola is suspected.|
|Clostridium difficile gastroenteritis||Contact||Duration of illness||Discontinue antibiotics if appropriate. Use soap and water for hand-washing, as antiseptic handrubs lack sporicidal activity. Do not share equipment (e.g., electronic thermometers). Ensure consistent environmental cleaning and disinfection.|
|Influenza, seasonal||Droplet||5 days after onset of symptoms||Single patient room preferred or cohort. Use mask on patient when he or she is transported out of room. Use gown and gloves according to Standard Precautions. The duration of precautions for immunocompromised patients cannot be defined. Refer to CDC guidance (http://www.cdc.gov/flu/professionals/infectioncontrol/healthcaresettings.htm).|
|Influenza, pandemic||Droplet||5 days after onset of symptoms||Refer to CDC guidance (http://www.cdc.gov/flu/pandemic-resources).|
|Influenza, avian||Droplet||Duration of illness||Refer to CDC guidance (http://www.cdc.gov/flu/avianflu).|
|Malaria||Standard||Ongoing||Install screens in windows and doors in endemic areas.|
|Measles (rubeola), all presentations||Airborne||4 days after onset of rash (duration of illness for immunocompromised patients )||Use Airborne Precautions for exposed susceptible patients. Susceptible healthcare staff should not enter the room if immune caregivers are available. Exclude susceptible healthcare staff from duty from day 5 after first exposure to day 21 after last exposure, regardless of post-exposure vaccine.|
|Meningitis (Haemophilus influenzae or Neisseria meningitidis [meningococcal] known or suspected)||Droplet||Until 24 hours after initiation of effective therapy||—|
|Meningococcal pneumonia||Droplet||Until 24 hours after initiation of effective therapy||—|
|Norovirus||Standard||Duration of illness||Cohorting of affected patients to separate airspaces and toilet facilities may help interrupt transmission during outbreaks. Use Contact Precautions for diapered or incontinent persons for the duration of illness or to control outbreaks. Ensure consistent environmental cleaning and disinfection, with focus on restrooms even when apparently unsoiled. Persons who clean heavily contaminated areas may benefit from wearing masks as virus can be aerosolized.|
|Plague, pneumonic||Droplet||Until 48 hours after initiation of effective therapy||Antimicrobial prophylaxis should be given to exposed healthcare staff.|
|Scabies||Contact||Until 24 hours after initiation of effective therapy||—|
|Group A streptococci, skin, wound, or burn (major: no dressing or dressing does not contain drainage adequately)||
|Until 24 hours after initiation of effective therapy||—|
|Toxic shock syndrome (staphylococcal or streptococcal disease)||Standard||Ongoing||—|
|Tuberculosis, extrapulmonary (draining lesion)||Airborne, Contact||Only when therapy is effective, patient is clinically improving, and the cultures of 3 consecutive sputum smears, collected on different days, are negative||Examine for evidence of active pulmonary tuberculosis. (If evidence exists, additional precautions are necessary.)|
|Tuberculosis, extrapulmonary, (no draining lesion, meningitis)||Standard||Ongoing||Examine for evidence of pulmonary tuberculosis. (If evidence exists, additional precautions are necessary.)|
|Tuberculosis, pulmonary or laryngeal disease (confirmed)||Airborne||Only when therapy is effective, patient is clinically improving, and the cultures of 3 consecutive sputum smears, collected on different days, are negative||—|
|Tuberculosis, pulmonary or laryngeal disease (suspected)||Airborne||Only when the likelihood of infectious disease is negligible and the cultures of 3 consecutive sputum smears, collected on different days, are negative||—|
|Tuberculosis, latent (skin-test positive with no evidence of current pulmonary disease)||Standard||Ongoing||—|
|Varicella zoster (chickenpox)||Airborne, Contact||Until all lesions are crusted (10 to 21 days) Susceptible healthcare staff should not enter the room if immune caregivers are available.|
|Whooping cough (pertussis)||Droplet||Until 5 days after initiation of effective therapy||—|
The following case outlines an investigative process and illustrates that the source of an outbreak may be unusual .
A cardiac surgeon noticed a cluster of cases of sternal wound dehiscence among his patients who had had surgery. Specimens from the wounds were obtained for culture. Microbiologic evaluation indicated that the infections were predominantly caused by Enterobacter cloacae, and molecular typing and serotyping demonstrated that the isolates were similar. No infections had developed after operations the surgeon had performed at other hospitals. No breach in aseptic technique was identified. All of the infected patients had been operated on in the same operating room, and the environment was screened. No source was found. Further questioning of the surgeon's operative practice revealed one difference from other cardiac surgeons: he used semi-frozen Hartmann's solution to achieve cardioplegia. Swabbing of the freezer used for the solution identified E. cloacae of the same typing as that found in the wound infections. The hypothesis was that contamination of the freezer led to contamination of the ice/slush solution, and the micro-organism was transmitted to the patients. The freezer was replaced, a rigorous cleaning schedule was instituted, and no further cases have occurred.
The following are overviews of selected potential outbreaks. Identification and early action in the case of any of these outbreaks will limit the adverse effects.
Most outbreaks of group A streptococci involve surgical wounds, and the source can usually be traced to an asymptomatic carrier in the operating room or on the wound care team [87,316]. Standard Precautions are sufficient if the wound is minor; if it is major, Contact Precautions should be instituted and followed for 24 hours after initiation of effective therapy . The healthcare worker should receive antimicrobial therapy as appropriate and leave the setting until completion of therapy.
Dealing with pulmonary tuberculosis involves prompt identification of the disease and determining the susceptible individuals who were exposed to the patient before isolation . Airborne Precautions should be instituted and remain in place until the patient is receiving effective therapy, is improving clinically, and the culture results for three consecutive sputum specimens, collected on different days, are negative. Comprehensive information is available in the CDC guidelines for preventing the transmission of tuberculosis in healthcare facilities .
The source of HAI with Legionella pneumonia is usually contaminated water . Implementation of Standard Precautions for the patient is sufficient . Laboratory-based surveillance for nosocomial Legionella should be performed, and samples of tap water should be obtained for culture. If the culture is positive, it is best to obtain cultures from patients who have healthcare-associated pneumonia. There are more than 40 known types of Legionella species, but most outbreaks are caused by Legionella pneumophila serotypes 1 and 6.
Outbreaks of antibiotic resistance have involved MRSA, VRE, and, most recently, vancomycin-resistant S. aureus . In such outbreaks, it is important to identify patients with colonization or infection early and isolate them or cohort them. Contact Precautions should be implemented and carried out until antibiotic therapy has been completed and cultures are negative . The importance of adhering to proper hand hygiene and other elements of Contact Precautions should be emphasized. Healthcare workers who were involved with patients before isolation should be evaluated for colonization and infection and treated appropriately.
The potential for other outbreaks or epidemics vary, and the CDC website, http://www.bt.cdc.gov, offers resources on emergency preparedness for outbreaks or epidemics caused by potential agents of bioterrorism, including anthrax and viral hemorrhagic fever. A Bioterrorism Readiness Plan template is also available (http://emergency.cdc.gov/bioterrorism/pdf/13apr99APIC-CDCBioterrorism.pdf). Many aspects should be considered when planning for bioterrorism preparedness, and each department of a healthcare facility can play an important role.
Infections acquired in the healthcare setting raise a great risk for patients, leading to high rates of morbidity and mortality. Many of the deaths caused by HAIs could be prevented by following evidence-based guidelines and consensus statements on prevention strategies. Several institutions have implemented campaigns to enhance the quality of health care and patient safety by focusing on measures to reduce the most common HAIs: catheter-associated urinary tract infection, surgical site infection, pneumonia, intravascular device-related bloodstream infection, and C. difficile infection. The single most effective infection control measure is appropriate hand hygiene, and all efforts to reduce the rate of HAIs must focus on enhancing compliance with this measure in conjunction with other prevention strategies. Along with hand hygiene, meticulous attention to aseptic technique when preparing for invasive procedures or using invasive devices is also essential for reducing the prevalence of HAIs. Prevention measures specific for each of the most common types of HAIs have been recommended in evidence-based guidelines and consensus statements (Table 20).
SUMMARY OF PREVENTION MEASURES FOR THE MOST COMMON HEALTHCARE-ASSOCIATED INFECTIONS
|Type of Infection||Evidence-Based Recommended Measures||Other Suggestions|
|Catheter-associated urinary tract infection||
|Pneumonia (without mechanical intubation)||
|Surgical site infection||
|Performance feedback to surgeons|
|Intravascular device- related bloodstream infections||
|Clostridium difficile-associated diarrhea||
|aComponent of a bundle of interventions that, when implemented together, has lowered the rate of infection.|
The common pathogens, diagnosis, and treatment vary among these infections and even within each type of infection. The CDC has detailed diagnostic criteria for each type of infection, and consensus statements and guidelines have also proposed such criteria. The treatment of HAIs varies according to the pathogen and the anatomic site. The prevailing principle is to use antibiotics judiciously, as the inappropriate use of antibiotics has led to an increasing number of resistant strains of bacteria. When using empiric antibiotic therapy, physicians should select an antibiotic on the basis of known pathogens in the healthcare facility as a whole, as well as on the specific unit within the facility.
An effective infection control team is critical to reducing the incidence of HAIs in a healthcare facility. All departments within a healthcare facility should be represented on this team to ensure widespread adherence to prevention measures. The responsibilities of an infection control team are to conduct surveillance of infections; ensure compliance with infection control guidelines, including those for management of drug-resistant organisms; and establish response and control plans for outbreaks and epidemics. Most important is the development of an organizational culture that fosters a focus on patient safety and emphasizes education on HAIs and infection control for healthcare workers and patients and their families.
1. Rothenberg BM, Marbella A, Pines E, et al. Prevention of Healthcare-Associated Infections. Closing the Quality Gap: Revisiting the State of the Science. Evidence Report/Technology Assessment No. 208. Rockville, MD: Agency for Healthcare Research and Quality, 2012.
2. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimating health care-associated infections and deaths in U.S. hospitals, 2002.Pub Health Rep. 2007;122(2):160-166.
3. Srinivasan A, Wise M, Bell M, et al. Vital signs: central line-associated blood stream infections—United States, 2001, 2008, 2009. MMWR. 2011;60(08):243-248.
4. Scott RD II. The Direct Medical Costs of Healthcare-Associated Infections in U.S. Hospitals and the Benefits of Prevention. Available at http://www.cdc.gov/HAI/pdfs/hai/Scott_CostPaper.pdf. Last accessed January 15, 2016.
5. Shojania KG, Duncan BW, McDonald KM, Wachter RM (eds). Making Health Care Safer II: An Updated Critical Analysis of the Evidence for Patient Safety Practices. Evidence Report/Technology Assessment No. 211. Rockville, MD: Agency for Healthcare Research and Quality; 2013.
6. Adams K, Corrigan JM (eds). Priority Areas for National Action: Transforming Health Care Quality. Washington, DC: The National Academies Press; 2003.
7. McCannon CJ, Hackbarth AD, Griffin FA. Miles to go: an introduction to the 5 Million Lives Campaign. Jt Comm J Qual Patient Safe. 2007;33(8):477-484.
8. U.S. Department of Health and Human Services. National Action Plan to Prevent Healthcare-Associated Infections: Road Map to Elimination. Available at http://health.gov/hcq/pdfs/hai-action-plan-executive-summary.pdf. Last accessed January 15, 2016.
9. Centers for Medicare & Medicaid Services. Medicare program: proposed and final changes to the hospital inpatient prospective payment systems and fiscal year 2009 rates. Fed Regist. 2008;73(161):48433-49084.
10. Centers for Medicare & Medicaid Services. CMS Improves Patient Safety for Medicare and Medicaid By Addressing Never Events. Available at https://www.cms.gov/Newsroom/MediaReleaseDatabase/Fact-sheets/2008-Fact-sheets-items/2008-08-042.html. Last accessed January 15, 2016.
11. National Quality Forum. Patient Safety. Available at www.qualityforum.org/Topics/Patient_Safety.aspx. Last accessed January 15, 2016.
12. The Joint Commission. 2015 National Patient Safety Goals. Available at http://www.jointcommission.org/assets/1/6/2015_NPSG_HAP.pdf. Last accessed January 15, 2016.
13. Bratzler DW, Hunt DR. The surgical infection prevention and surgical care improvement projects: national initiatives to improve outcomes for patients having surgery. Clin Infect Dis. 2006;43(3):322-330.
14. U.S. Department of Health and Human Services. National Action Plan to Prevent Healthcare-Associated Infections: Roadmap to Elimination. Available at http://www.hhs.gov/ash/initiatives/hai/exec_summary.html. Last accessed January 15, 2016.
15. World Health Organization. Prevention of Hospital-Acquired Infections. A Practical Guide. 2nd ed. Geneva: WHO Press; 2002.
16. Mehta AC, Prakash UB, Garland R, et al. American College of Chest Physicians and American Association for Bronchology consensus statement: prevention of flexible bronchoscopy-associated infection. Chest. 2005;128(3):1742-1755.
17. American Thoracic Society, Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med. 2005;171(4):388-416.
18. Facility Guidelines Institute and American Society for Healthcare Engineer. Guidelines for Design and Construction of Hospitals and Outpatient Facilities. American Hospital Association: Lakewood, CO; 2014.
19. Dodek P, Keenan S, Cook D, et al., for the Canadian Critical Care Trials Group and the Canadian Critical Care Society. Evidence-based clinical practice guideline for the prevention of ventilator-associated pneumonia. Ann Intern Med. 2004;141(4):305-313.
20. Gould CV, Umscheid CA, Agarwal RK, Kuntz G, Pegues DA, Healthcare Infection Control Practices Advisory Committee. Guideline for Prevention of Catheter-Associated Urinary Tract Infections, 2009. Available at http://www.cdc.gov/hicpac/cauti/002_cauti_toc.html. Last accessed January 15, 2016.
21. Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for Disinfection and Sterilization in Healthcare Facilities, 2008. Available at http://www.cdc.gov/hicpac/Disinfection_Sterilization/acknowledg.html. Last accessed January 15, 2016.
22. Siegel JD, Rhinehart E, Jackson M, Chiarello L, and the Healthcare Infection Control Practices Advisory Committee. 2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Healthcare Settings. Available at http://www.cdc.gov/hicpac/2007IP/2007isolationPrecautions.html. Last accessed January 15, 2016.
23. Siegel JD, Rhinehart E, Jackson M, Chiarello L, the Healthcare Infection Control Practices Advisory Committee. Management of Multidrug-Resistant Organisms in Healthcare Settings, 2006. Available at http://www.cdc.gov/hicpac/mdro/mdro_toc.html. Last accessed January 15, 2016.
24. Tablan OC, Anderson LJ, Besser R, Bridges C, Hajjeh R. Guidelines for preventing health-care-associated pneumonia, 2003: recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee. MMWR. 2004;53(RR03):1-36.
25. Sehulster L, Chinn RYW. Guidelines for environmental infection control in health-care facilities. MMWR. 2003;52(RR10):1-42.
26. Boyce JM, Pittet D. Guideline for hand hygiene in health-care settings. MMWR. 2002;51(RR16):1-44.
27. O'Grady NP, Alexander M, Burns LA, et al. Guidelines for the Prevention of Intravascular Catheter-Related Infections, 2011. Available at http://www.guideline.gov/content.aspx?id=34426. Last accessed January 15, 2016.
28. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR, The Hospital Infection Control Practices Advisory Committee. Guideline for Prevention of Surgical Site Infection, 1999. Available at http://www.cdc.gov/hicpac/SSI/001_SSI.html. Last accessed January 15, 2016.
29. Hooton TM, Bradley SF, Cardenas DD, et al. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 international clinical practice guidelines from the Infectious Diseases Society of America. Clin Infect Dis. 2010;50(5):625-663.
30. Muto CA, Jernigan JA, Ostrowsky BE, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and Enterococcus. Infect Control Hosp Epidemiol. 2003;24(5):362-386
31. Nelson DB, Jarvis WR, Rutala WA, et al. Multi-society guideline for reprocessing flexible gastrointestinal endoscopes. Infect Cont Hosp Epidemiol. 2003;24(7):532-537.
32. Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infect Cont Hosp Epidemiol. 2010;31(5):431-455.
33. Shlaes DM, Gerding DN, John JF Jr, et al. Society for Healthcare Epidemiology of America and Infectious Diseases Society of America Joint Committee on the Prevention of Antimicrobial Resistance: guidelines for the prevention of antimicrobial resistance in hospitals. Infect Cont Hosp Epidemiol. 1997;18(4):275-291.
34. Marschall J, Mermel LA, Classen D, et al. Strategies to prevent central-line-associated bloodstream infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29(suppl 1):S62-S80.
35. Coffin SE, Klompas M, Classen D, et al. Strategies to prevent ventilator-associated pneumonia in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29(suppl 1):S22-S30.
36. Lo E, Nicolle L, Classen D, et al. Strategies to prevent catheter-associated urinary tract infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29:S41-S50.
37. Anderson DJ, Kaye KS, Classen D, et al. Strategies to prevent surgical site infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29:S51-S61.
38. Calfee DP, Salgado CD, Classen D, et al. Strategies to prevent transmission of methicillin-resistant Staphylococcus aureus in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29:S62-S80.
40. Clark AP, Houston S. Nosocomial infections: an issue of patient safety: part 2. Clin Nurse Spec. 2004;18(2):62-64.
41. Pittet D, Hugonnet S, Harbarth S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Infection Control Programme. Lancet. 2000;356(9238):1307-1312.
42. Larson EL, Quiros D, Lin SX. Dissemination of the CDC's Hand Hygiene Guideline and impact on infection rates. Am J Infect Control. 2007;35(10):666-675.
43. Craven DE, Hjalmarson K. Prophylaxis of ventilator-associated pneumonia: changing culture and strategies to trump disease.Chest. 2008;134(5):898-900.
44. Brown J, Doloresco F III, Mylotte JM. "Never events:" not every hospital-acquired infection is preventable. Clin Infect Dis. 2009;49:743-746.
45. Haley RW. Managing Hospital Infection Control for Cost-Effectiveness. Chicago, IL: American Hospital Association; 1986.
46. Babcock HM, Woeltie KF. The development of infection surveillance and control programs. In: Bennett JV, Brachman PS (eds). Hospital Infections. Philadelphia, PA: Lipincott, Williams, and Wilkins; 2014: 57-62.
47. Harbarth S, Sax H, Gastmeier P. The preventable proportion of nosocomial infections: an overview of published reports. J Hosp Infect. 2003;54(4):258-266.
48. Umscheid CA, Mitchell MD, Doshi JA, et al. Estimating the proportion of healthcare-associated infections that are reasonably preventable and the related mortality and costs. Infect Control Hosp Epidemiol. 2011;32(2):101-114.
49. Hedrick TL, Heckman JA, Smith RL, Sawyer RG, Friel CM, Foley EF. Efficacy of protocol implementation on incidence of wound infection in colorectal operations. J Am Coll Surg. 2007;205(3):432-438.
50. Hawn MT, Itani KM, Gray SH, Vick CC, Henderson W, Houston TK. Association of timely administration of prophylactic antibiotics for major surgical procedures and surgical site infection. J Am Coll Surg. 2008;206(5):814-819.
51. Pastor C, Artinyan A, Varma MG, Kim E, Gibbs L, Garcia-Qquilar J. An increase in compliance with the Surgical Care Improvement Project measures does not prevent surgical site infection in colorectal surgery. Dis Colon Rectum. 2010;53(1):24-30.
52. Krein SL, Kowalski CP, Hofer TP, Saint S. Preventing hospital-acquired infections: a national survey of practices reported by U.S. hospitals in 2005 and 2009. J Gen Intern Med. 2012;27(7):773-779.
53. Morris AC, Hay AW, Swann DG, et al. Reducing ventilator-associated pneumonia in intensive care: impact of implementing a care bundle. Crit Care Med. 2011;39(10):2218-2224.
54. Zack J. Zeroing in on zero tolerance for central line-associated bactermia. Am J Infect Control. 2008;36(10):S176:e1-e2.
55. Galpern D, Guerrero A, Tu A, Fahoum B, Wise L. Effectiveness of a central line bundle campaign on line-associated infections in the intensive care unit. Surgery. 2008;144(4):492-495.
56. Pronovost P, Needham D, Berenholtz S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU.N Engl J Med. 2006;355(26):2725-2732.
57. Yokoe DS, Classen. Improving patient safety through infection control: a new healthcare imperative. Infect Control Hosp Epidemiol. 2008;29(suppl 1):S3-S11.
58. Curtis LT. Prevention of hospital-acquired infections: review of non-pharmacological interventions. J Hosp Infect. 2008;69(3):204-219.
59. Institute for Healthcare Improvement. 5 Million Lives Campaign. Available at http://www.ihi.org/Engage/Initiatives/Completed/5MillionLivesCampaign/Pages/default.aspx. Last accessed January 15, 2016.
60. Lee GM, Kleinman K, Soumerai SB, et al. Effect of nonpayment for preventable infections in U.S. hospitals. N Engl J Med. 2012;367(15):1428-1437.
61. Lee GM, Hartmann CW, Graham D, et al. Perceived impact of the Medicare policy to adjust payment for health care-associated infections. Am J Infect Control. 2012;40(4):314-319.
62. Edmond M, Eickhoff TC. Who is steering the ship? External influences on infection control programs. Clin Infect Dis. 2008;46(11):1746-1750.
63. Safdar N, Abad C. Educational interventions for prevention of healthcare-associated infection: a systematic review. Crit Care Med. 2008;36(3):933-940.
64. Welsh CA, Flanagan ME, Hoke SC, Doebbeling BN, Herwaldt L, Reducing health care-associated infections (HAIs): lessons learned from a national collaborative of regional HAI programs. Am J Infect Control. 2012;40(1):29-34.
65. Edwards JR, Peterson KD, Andrus ML, et al. National Healthcare Safety Network (NHSN) Report, data summary for 2006, issued June 2007. Am J Infect Control. 2007;35(5):290-301.
66. Centers for Disease Control and Prevention. National Healthcare Safety Network (NHSN). Available at http://www.cdc.gov/nhsn/. Last accessed January 15, 2016.
67. Centers for Disease Control and Prevention, Association of State and Territorial Health Officials. Eliminating Healthcare-Associated Infections. State Policy Options. Arlington, VA: Association of State and Territorial Health Officials; 2011.
68. Centers for Disease Control and Prevention. State-Based HAI Prevention. Available at http://www.cdc.gov/hai/stateplans/required-to-report-hai-NHSN.html. Last accessed January 15, 2016.
70. Pier G. Molecular mechanisms of microbial pathogenesis. In: Kasper D, Fauci AS, Hauser SL, Longo DL, Jameson JL, Loscalzo J (eds). Harrison's Principles of Internal Medicine. 19th ed. New York: McGraw Hill; 2015.
71. Dellit TH, Owens RC, McGowan JE, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44(2):159-177.
72. Calfee DP, Salgado CD, Milstone AM, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(7):772-796.
73. Joint Commission Accreditation. Comprehensive Accreditation Manual 2015: Standards of Elements of Performance Scoring Accreditation Policies (Comprehensive Accreditation Manual for Hospitals [CAMH]). Oakbrook Terrace, IL: Joint Commission on Accreditation of Healthcare Organizations; 2014.
74. Spellberg B, Guidos R, Gilbert D, et al. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clin Infect Dis. 2008;46(2):155-164.
75. Boucher HW, Talbot GH, Bradley JS, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1-12.
76. Boucher HW, Talbot GH, Benjamin DK Jr, et al. 10 x '20 progress – development of new drugs active against gram-negative bacilli: an update from the Infectious Diseases Society of America. Clin Infect Dis. 2013;56(12):1685-1694.
77. Safdar N, Maki DG. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, Enterococcus, gram-negative bacilli, Clostridium difficile, and Candida. Ann Intern Med. 2002;136(11):834-844.
78. Sydnor ERM, Perl TM. Hospital epidemiology and infection control in acute-care settings. Clin Microbiol Rev. 2011;24(1):141-173.
79. Raymond DP, Pelletier SJ, Crabtree TD, Evans HL, Pruett TL, Sawyer RG. Impact of antibiotic-resistant gram-negative bacilli infections on outcome in hospitalized patients. Crit Care Med. 2003;31(4):1035-1041.
80. Roberts RR, Hota B, Ahmad I, et al. Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clin Infect Dis. 2009;49(8):1175-1184.
81. Sievert DM, Ricks P, Edwards JR, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol. 2013;34(1):1-14.
82. Schwaber MJ, Carmeli Y. Carbapenem-resistant Enterobacteriaceae: a potential threat. JAMA. 2008;300(24):2911-2913.
83. Lledo W, Hernandez M, Lopez E, et al. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR. 2009;58(10):256-260.
84. Liu C, Bayer A, Cosgrove SE, et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis. 2011;52(3):e18-e55.
85. Clark AP, John LD. Nosocomial infections and bath water: any cause for concern? Clin Nurse Spec. 2006;20(3):119-123.
86. Anaissie EJ, Penzak SR, Dignani MC. The hospital water supply as a source of nosocomial infections: a plea for action. Arch Intern Med. 2002;162(13):1483-1492.
87. Weinstein R. Hospital-acquired infections. In: Kasper DL, Fauci AS, Hauser SL, Longo DL, Jameson JL, Loscalzo J (eds.) Harrison's Principles of Internal Medicine. 19th ed. New York: McGraw Hill; 2015.
88. Perdelli F, Cristina ML, Sartini M, et al. Fungal contamination in hospital environments. Infect Cont Hosp Epidemiol. 2006;27(1):44-47.
89. Noskin GA, Peterson LR. Engineering infection control through facility design. Emerg Infect Dis. 2001;7(2):354-357.
90. Passweg JR, Rowlings PA, Atkinson KA, et al. Influence of protective isolation on outcome of allogeneic bone marrow transplantation for leukemia. Bone Marrow Transplant. 1998;21(12):1231-1238.
91. Centers for Disease Control and Prevention. Guidelines for preventing opportunistic infections among hematopoietic stem cell transplant recipients. MMWR. 2000; 49(RR1-10):1-125.
92. Yokoe D, Casper C, Dubberke E, et al. Infection prevention and control in health-care facilities in which hematopoietic cell transplant recipients are treated. Bone Marrow Transplant. 2009;44(8):495-507.
93. Streifel AJ, Hendrickson C. Assessment of health risks related to construction: minimizing the threat of infection from construction-induced air pollution in health-care facilities. HPAC Engineering. 2002:27-32.
94. Ortolano GA, McAlister MB, Angelbeck JA, et al. Hospital water point-of-use filtration: a complementary strategy to reduce the risk of nosocomial infection. Am J Infect Control. 2005;33(5 Suppl 1):S1-S19.
95. Reuter S, Sigge A, Wiedeck H, Trautmann M. Analysis of transmission pathways of Pseudomonas aeruginosa between patients and tap water outlets. Crit Care Med. 2002;30(10):2222-2228.
96. Pier GB, Ramphal R. Pseudomonas aeruginosa. In: Mandell GL, Bennett JE, Dolin R (eds). Principles and Practices of Infectious Diseases, 7th ed. Philadelphia, PA: Churchill Livingstone Elsevier; 2010.
97. Agency for Healthcare Research and Quality. 10 Patient Safety Tips for Hospitals. Available at http://www.ahrq.gov/patients-consumers/diagnosis-treatment/hospitals-clinics/10-tips/index.html. Last accessed January 15, 2016.
98. Detsky ME, Etchells E. Single-patient rooms for safe patient-centered hospitals. JAMA. 2008;300(8):954-956.
99. Whitby M, McLaws ML. Handwashing in healthcare workers: accessibility of sink location does not improve compliance. J Hosp Infect. 2004;58(4):247-253.
100. Favero MS, Bond WW. Disinfection of medical and surgical materials. In: Block SS (ed). Disinfection, Sterilization, and Preservation. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2001: 881-917.
101. American Society for Gastrointestinal Endoscopy. Infection control during gastrointestinal endoscopy. Gastrointest Endosc. 2008;67(6):781-790.
102. Spach DH, Silverstein FE, Stamm WE. Transmission of infection by gastrointestinal endoscopy and bronchoscopy. Ann Intern Med. 1993;118(2):117-128.
103. Muscarella LF. Inconsistencies in endoscope-reprocessing and infection-control guidelines: the importance of endoscope drying.Am J Gastroenterol. 2006;101(9):2147-2154.
104. U.S. Food and Drug Administration. Infections Associated with Reprocessed Flexible Bronchoscopes: FDA Safety Communication. Available at http://www.fda.gov/MedicalDevices/Safety/AlertsandNotices/ucm462949.htm. Last accessed January 15, 2016.
105. Culver DA, Gordon SM, Mehta AC. Infection control in the bronchoscopy suite: a review of outbreaks and guidelines for prevention. Am J Respir Crit Care Med. 2003;167(8):1050-1056.
106. Srinivasan A, Wolfenden LL, Song X, et al. An outbreak of Pseudomonas aeruginosa infections associated with flexible bronchoscopes. N Engl J Med. 2003;348(3):221–227.
107. Kirschke DL, Jones TF, Craig AS, Chu PS, Mayernick GG, Patel JA, Schaffner W. Pseudomonas aeruginosa and Serratia marcescens contamination associated with a manufacturing defect in bronchoscopes. N Engl J Med. 2003;348(3)214-220.
108. Nelson DB, Muscarella LF. Current issues in endoscope reprocessing and infection control during gastrointestinal endoscopy.World J Gastroenterol. 2006;12(25):3953-3964.
109. Leung JW. Reprocessing of flexible endoscopes. J Gastroenterol Hepatol. 2000;15(Suppl):G73-G77.
110. Kovaleva J, Peters FTM, van der Mei H, Degener JE. Transmission of infection by flexible gastrointestinal endoscopy and bronchoscopy. Clin Microbiol Rev. 2013;26(2):231-254.
111. Schabrun S, Chipchase L. Healthcare equipment as a source of nosocomial infection: a systematic review. J Hosp Infect. 2006;63(3):239-245.
112. Bernard L, Kereveur A, Durand D, et al. Bacterial contamination of hospital physicians' stethoscopes. Infect Control Hosp Epidemiol. 1999;20(9):626-628.
113. Lecat P, Cropp E. McCord G, Haller NA. Ethanol-based cleanser versus isopropyl alcohol to decontaminate stethoscopes.Am J Infect Control. 2009;37(3):241-243.
114. Schroeder A, Schroeder MA, D'Amico F. What's growing on your stethoscope? (And what you can do about it). J Fam Pract. 2009;58(8):404-409.
115. Russell A, Secrest J, Schreeder C. Stethoscopes as a source of hospital-acquired methicillin-resistant Staphylococcus aureus. J Peranesth Nurs. 2012;27(2):82-87.
116. Schabrun S, Chipchase L, Rickard H. Are therapeutic ultrasound units a potential vector for nosocomial infection? Physiother Res Int. 2006;11(2):61-71.
117. Hausermann P, Widmer A, Itin P. Dermatoscope as vector for transmissible diseases-no apparent risk of nosocomial infections in outpatients. Dermatology. 2006;212(1):27-30.
118. Kelly SC, Purcell SM. Prevention of nosocomial infection during dermoscopy? Dermatol Surg. 2006;32(4):552-555.
119. Devine J, Cooke RP, Wright EP. Is methicillin-resistant Staphylococcus aureus (MRSA) contamination of ward-based computer terminals a surrogate marker for nosocomial MRSA transmission and handwashing compliance? J Hosp Infect. 2001;48(1):72-75.
120. Vinh DC, Embil JM. Device-related infections: a review. J Long-Term Effects Med Implants. 2005;15(5):467-488.
121. Harris LG, Richards RG. Staphylococci and implant surfaces: a review. Injury. 2006;37(Suppl 2):S3-S14.
122. Schierholz JM, Beuth J. Implant infections: a haven for opportunistic bacteria. J Hosp Infect. 2001;49(2):87-93.
123. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36(5):309-332.
124. Anderson DJ, Podgomy K, Berrios-Torres SI, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(6):605-627.
125. Mittmann N, Koo M, Daneman N, et al. The economic burden of patient safety targets in acute care: a systematic review. Drug, Healthcare Patient Safe. 2012;4:141-165.
126. Dubberke ER, Butler AM, Yokoe DS, et al. Multicenter study of Clostridium difficile infection rates from 2000 to 2006. Infect Control Hosp Epidemiol. 2010;31(10):1030-1037.
127. Dubberke ER, Olsen MA. Burden of Clostridium difficile on the healthcare system. Clin Infect Dis. 2012;55(Suppl 2):S88-S92.
128. Mitchell BG, Gardner A. Mortality and Clostridium difficile infection: a review. Antimicrob Resist Infect Control. 2012;1(1):20.
129. McGlone SM, Bailey RR, Zimmer SM, et al. The economic burden of Clostridium difficile. Clin Microbiol Infect. 2012;18(3):282-289.
130. Weber DJ, Sickbert-Bennett EE, Gould CV, Brown VM, Huslage K, Rutala WA. Incidence of catheter-associated and non-catheter-associated urinary tract infections in a healthcare system. Infect Control Hosp Epidemiol. 2011;32:822–823.
131. Lo E, Nicolle LE, Coffin SE, et al. Strategies to prevent catheter-associated urinary tract infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(5):464-479.
133. Chen HS, Wang FD, Lin M, Lin YC, Huang LJ, Liu CY. Risk factors for central venous catheter-related infections in general surgery. J Microbiol Immunol Infect. 2006;39(3):231-236.
134. Mukhtar RA, Throckmorton AD, Alvarado MD, et al. Bacteriologic features of surgical site infections following breast surgery.Am J Surg. 2009;198(4):529-531.
135. Dalstrom DJ, Venkatarayappa I, Manternach AL, Palcic MS, Heyse BA, Prayson MJ. Time-dependent contamination of opened sterile operating-room trays. J Bone Joint Surg Am. 2008;90(5):1022-1025.
136. de Wit M, Goldberg S, Hussein E, Neifeld JP. Health care-associated infections in surgical patients undergoing elective surgery: are alcohol use disorders a risk factor? J Am Coll Surg. 2012;215(2):229-236.
137. Qaseem A, Snow V, Fitterman N, et al. Risk assessment for and strategies to reduce perioperative pulmonary complications for patients undergoing noncardiothoracic surgery: a guideline from the American College of Physicians. Ann Intern Med. 2006;144(8):575-580.
138. Eom C-S, Jeon CY, Cho E-G, Park SM, Lee K-S. Use of acid-suppressive drugs and risk of pneumonia: a systematic review and meta-analysis. CMAJ. 2011;183(3):310-319.
139. Merle V, Hallais C, Tavolacci MP, et al. Validity of medical staff assessment at admission of patient's risk of nosocomial infection: a prospective study in a surgical intensive care unit. Intensive Care Med. 2006;32(6):915-918.
140. Dudeck MA, Weiner LM, Allen-Bridson K, et al. National Healthcare Safety Network (NHSN) report, data summary for 2012, device-associated module. Am J Infect Cont. 2013;41:1148-1166.
141. Centers for Disease Control and Prevention. Healthcare-Associated Infections (HAIs). HAI Prevalence Survey. Available at http://www.cdc.gov/HAI/surveillance/index.html. Last accessed January 15, 2016.
142. Magill SS, Edwards JR, Bamberg W, et al. Multistate point-prevalence survey of health care-associated infections. New Engl J Med. 2014;370:1198-1208.
143. Wald HL, Ma A, Bratzler DW, et al. Indwelling urinary catheter use in the postoperative period: analysis of the National Surgical Infection Prevention Project data. Arch Surg. 2008;143(6):551-557.
144. Srinivasan A, Karchmer T, Richards A, Song X, Perl TM. A prospective trial of a novel, silicone-based, silver-coated foley catheter for the prevention of nosocomial urinary tract infections. Infect Control Hosp Epidemiol. 2006;27(1):38-43.
145. Johnson JR, Kuskowski MA, Witt TJ. Systematic review: antimicrobial urinary catheters to prevent catheter-associated urinary tract infection in hospitalized patients. Ann Intern Med. 2006;144(2):116-126.
146. Beattie M, Taylor J. Silver alloy vs. uncoated urinary catheters: a systematic review of the literature. J Clin Nurs. 2011;20(15-16):2098-2108.
147. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaffer A, Hooton TM. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis. 2005;40(5):643-654.
148. Buonanno AP Jr, Damweber BJ. Review of urinary tract infection. US Pharm. 2006;31(6):HS26-HS36.
149. Fink R, Gilmartin H, Richard A, et al. Indwelling urinary catheter management and catheter-associated urinary tract infection prevention practices in Nurses Improving Care for Healthsystem Elders hospitals. Am J Infect Control. 2012;40(8):715-720.
150. Saint S, Wiese J, Amory JK, et al. Are physicians aware of which of their patients have indwelling urinary catheters? Am J Med. 2000;109(6):476-480.
151. Saint S, Kowalski CP, Kaufman SR, et al. Preventing hospital-acquired urinary tract infection in the United States: a national study. Clin Infect Dis. 2008;46(2):243-250.
152. Conway LJ, Pogorzelska M, Larson E, Stone PW. Adoption of policies to prevent catheter-associated urinary tract infections in United States intensive care units. Am J Infect Control. 2012;40(8):705-710.
153. Topal J, Conklin S, Camp K, Morris V, Balcezak T, Herbert P. Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol. Am J Med Qual. 2005;20(3):121-126.
154. Saint S, Kaufman SR, Thompson M, Rogers MA, Chenoweth CE. A reminder reduces urinary catheterization in hospitalized patients. Jt Comm J Qual Patient Saf. 2005;31(8):455-462.
155. Burton DC, Edwards JR, Srinivasan A. Fridkin SK, Gould CV. Trends in catheter-associated urinary tract infections in adult intensive care units—United States, 1990–2007. Infect Control Hosp Epidemiol. 2011;32(8):748-756.
156. Fuchs MA, Sexton DJ, Thornlow DK, Champagne MT. Evaluation of an evidence-based, nurse-driven checklist to prevent hospital-acquired catheter-associated urinary tract infections in intensive care units. J Nurse Care Qual. 2011;26(2):101-109.
157. Centers for Disease Control and Prevention. FastStats: Inpatient Surgery. Available at http://www.cdc.gov/nchs/fastats/inpatient-surgery.htm. Last accessed January 15, 2016.
158. Stevens DL, Bisno AL, Chambers HF, et al. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis. 2014;59(2):e10-e52.
159. Nan DN, Fernandez-Ayala M, Farinas-Alvarez C, et al. Nosocomial infection after lung surgery: incidence and risk factors. Chest. 2005;128(4):2647-2652.
160. de Lissovoy G, Fraeman K, Hutchins V, et al. Surgical site infection: incidence and impact on hospital utilization and treatment costs. Am J Infect Control. 2009;37(5):387-397.
161. McGarry SA, Engemann JJ, Schmader K, Sexton DJ, Kaye KS. Surgical-site infection due to Staphylococcus aureus among elderly patients: mortality, duration of hospitalization, and cost. Infect Control Hosp Epidemiol. 2004;25(6):461-467.
162. Centers for Disease Control and Prevention. Healthcare-Associated Infections (HAI) Progress Report. Available at http://www.cdc.gov/hai/progress-report/index.html. Last accessed January 15, 2016.
163. Hawn MT, Vick CC, Richman J, et al. Surgical site infection prevention: time to move beyond the surgical care improvement program. Ann Surg. 2011;254(3):494-499.
164. Cheadle W. Risk factors for surgical site infection. Surg Infect(Larchmt). 2006;7(Suppl 1):s7-s11.
165. Manilich E, Vogel JD, Kiran RP, Church JM, Seyidova-Khoshknabi D, Remzi FH. Key factors associated with postoperative complications in patients undergoing colorectal surgery. Dis Colon Rectum. 2013;56(1):64-71.
166. Berrios-Torres SI, Umscheid CA, Bratzler DW, et al. Draft Guidelines for the Prevention of Surgical Site Infection. Available at http://www.jscva.org/files/CDC-SSI_Guideline_Draft2014.pdf. Last accessed January 15, 2016.
167. Bratzler DW, Houck PM. Antimicrobial prophylaxis for surgery: an advisory statement from the National Surgical Infection Prevention Project. Clin Infect Dis. 2005;189(4):395-404.
168. Auerbach AD. Prevention of surgical site infections. In: Shojania KG, Duncan BW, McDonald KM, Wachter RM (eds). Making Health Care Safer A Critical Analysis of Patient Safety Practices. Evidence Report/Technology Assessment, No. 43. Rockville, MD: Agency for Healthcare Research and Quality; 2001.
169. Webster J, Osborne S. Preoperative bathing or showering with skin antiseptics to prevent surgical site infection. Cochrane Database Syst Rev. 2012;19(2):CD004985.
170. Tanner J, Woodings D, Moncaster K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev. 2006;19(2):CD004122.
171. Tanner J, Norrie P, Melen K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev. 2011;9(11):CD004122.
172. Awad SS, Palacio CH, Subramanian A, et al. Implementation of a methicillin-resistant Staphylococcus aureus (MRSA) prevention bundle results in decreased MRSA surgical site infections. Am J Surg. 2009;198(5):607-610.
173. Stevens DL, Bisno AL, Chambers HF, et al. Practice guidelines for the diagnosis and management of skin and soft-tissue infections. Clin Infect Dis. 2005;41(10):1373-1406.
174. Centers for Disease Control and Prevention. Surgical Site Infection (SSI) Event. Available at http://www.cdc.gov/nhsn/PDFs/pscManual/9pscSSIcurrent.pdf. Last accessed January 15, 2016.
175. Trampuz A, Widmer AF. Infections associated with orthopedic implants. Curr Opin Infect Dis. 2006;19(4):349-356.
176. Trampuz A, Zimmerli W. Antimicrobial agents in orthopaedic surgery: prophylaxis and treatment. Drugs. 2006;66(8):1089-1105.
177. Nguyen N, Yegiyants S, Kaloostian C, et al. The Surgical Care Improvement Project (SCIP) initiative to reduce infection in elective colorectal surgery: which performance measures affect outcome? Am Surg. 2008;74(10):1012-1016.
178. Ho VP, Barie PS, Stein SL, et al. Antibiotic regimen and the timing of prophylaxis are important for reducing surgical site infection after elective abdominal colorectal surgery. Surg Infect(Larchmt). 2011;12(4):255-260.
179. Berenguer CM, Ochsner MG Jr, Lord SA, Senkowski CK. Improving surgical site infections: using National Surgical Quality Improvement Program data to institute Surgical Care Improvement Project protocols in improving surgical outcomes. J Am Coll Surg. 2010;210(5):734-741.
180. Smith BP, Fox N, Fakhro A, et al. "SCIP"ping antibiotic prophylaxis guidelines in trauma: the consequences of noncompliance.J Trauma Acute Care Surg. 2012;73(2):452-456.
181. Edmiston CE, Spencer M, Lewis BD, et al. Reducing the risk of surgical site infections: did we really think SCIP was going to lead us to the promised land? Surg Infect (Larchmt). 2011;12(3):169-177.
182. Awad SS. Adherence to Surgical Care Improvement Project measures and post-operative surgical site infections. Surg Infect (Larchmt). 2012;13(4):234-237.
183. Schwann NM, Bretz KA, Eid S, et al. Point-of-care electronic prompts: an effective means of increasing compliance, demonstrating quality, and improving outcome. Anesth Analg. 2011;113(4):869-876.
184. 184. How-to Guide: Prevent Surgical Site Infections. Cambridge, MA: Institute for Healthcare Improvement; 2012.
185. Kollef MH. What is ventilator-associated pneumonia and why is it important? Respir Care. 2005;50(6):714-721.
186. Kieninger AN, Lipsett PA. Hospital-acquired pneumonia: pathophysiology, diagnosis, and treatment. Surg Clin North Am. 2009;89(2):439-461.
187. Pogorzelska M, Stone PW, Furuya EY, et al. Impact of the ventilator bundle on ventilator-associated pneumonia in intensive care unit. Int J Qual Health Care. 2011;23(5):538-544.
188. Dudeck MA, Weiner LM, Allen-Bridson K, et al. National Healthcare Safety Network (NHSN) report, data summary for 2012, device-associated module. Am J Infect Cont. 2014;41:1148-1166.
189. Tedja R, Gordon S. Hospital-Acquired, Health Care-Associated, and Ventilator-Associated Pneumonia. Available at http://www.clevelandclinicmeded.com/medicalpubs/diseasemanagement/infectious-disease/health-care-associated-pneumonia/#top. Last accessed January 15, 2016.
190. Kollef MH. Antibiotic management of ventilator-associated pneumonia due to antibiotic-resistant gram-positive bacterial infection. Eur J Clin Microbiol Infect Dis. 2005;24(12):794-803.
191. Kollef MH, Morrow LE, Niederman MS, et al. Clinical characteristics and treatment patterns among patients with ventilator-associated pneumonia. Chest. 2006;129(5):1210-1218.
192. Hidron AI, Edwards JR, Patel J, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol. 2008;29(11):996-1011.
193. Flanders SA, Collard HR, Saint S. Nosocomial pneumonia: state of the science. Am J Infect Control. 2006;34(2):84-93.
194. Kress JP, Pohlman AS, O'Connor MF, Hall JB. Daily interruption of sedative infusions in critically ill patients undergoing mechanical ventilation. N Engl J Med. 2000;342(20):1471-1477.
195. Schweickert WD, Gehlbach BK, Pohlman AS, Hall JB, Kress JP. Daily interruption of sedative infusions and complications of critical illness in mechanically ventilated patients. Crit Care Med. 2004;32(6):1272-1276.
196. Bearman GML, Munro C, Sessler CN, Wenzel RP. Infection control and the prevention of noscomial infections in the intensive care unit. Semin Respir Crit Care Med. 2006;27(3):310-324.
197. Drakulovic MB, Torres A, Bauer TT, et al. Supine body position as a risk factor for nosocomial pneumonia in mechanically ventilated patients: a randomised trial. Lancet. 1999;354(9193):1851-1858.
198. Shay A, O'Malley P. Blue Ribbon Abstract Award: Clinical outcomes of a ventilator associated pneumonia prevention program. Am J Infect Control. 2006;34(5):E19-E20.
199. El-Solh AA, Pietrantoni C, Bhat A, et al. Colonization of dental plaques: a reservoir of respiratory pathogens for hospital-acquired pneumonia in institutionalized elders. Chest. 2004;126(5):1575-1582.
200. Pineda LA, Saliba RG, El Solh AA. Effect of oral decontamination with chlorhexidine on the incidence of nosocomial pneumonia: a meta-analysis. Crit Care. 2006;10(1):R35.
201. Sona CS, Zack JE, Schallom ME, et al. The impact of a simple, low-cost oral care protocol on ventilator-associated pneumonia rates in a surgical intensive care unit. J Intensive Care Med. 2009;24(1):54-62.
202. Munro CL, Grap MJ, Jones DJ, McClish DK, Sessler CN. Chlorhexidine, toothbrushing, and preventing ventilator-associated pneumonia in critically ill adults. Am J Crit Care. 2009;18(5):428-437.
203. Geerts WH, Pineo GF, Heit JA, et al. Prevention of venous thromboembolism: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest. 2004;126(3 Suppl):338S-400S.
204. Pileggi C, Bianco A, Flotta D, Nobile CG, Pavia M. Prevention of ventilator-associated pneumonia, mortality and all intensive care unit acquired infections by topically applied antimicrobial or antiseptic agents: a meta-analysis of randomized controlled trials in intensive care units. Crit Care. 2011;15(3):R155.
205. Dezfulian C, Shojania K, Collard HR, Kim HM, Matthay MA, Saint S. Subglottic secretion drainage for preventing ventilator-associated pneumonia: a meta-analysis. Am J Med. 2005;118(1):11-18.
206. Bouza E, Perez MJ, Munoz, Rincon C, Barrio JM, Hortal J. Continuous aspiration of subglottic secretions in the prevention of ventilator-associated pneumonia in the postoperative period of major heart surgery. Chest. 2008;134(5):938-946.
207. Wang F, Bo L, Tang L, et al. Subglottic secretion drainage for preventing ventilator-associated pneumonia: an updated meta-analysis of randomized controlled trials. J Trauma Acute Care Surg. 2012;72(5):1276-1285.
208. Osmon S, Kollef MH. Prevention of pneumonia in the hospital setting. Clin Chest Med. 2005;26(1):135-142.
209. Isakow W, Kollef MH. Preventing ventilator-associated pneumonia: an evidence-based approach of modifiable risk factors. Semin Respir Crit Care Med. 2006;27(1):5-17.
210. Girou E, Brun-Buisson C, Taille S, Lemaire F, Brochard L. Secular trends in nosocomial infections and mortality associated with noninvasive ventilation in patients with exacerbation of COPD and pulmonary edema. JAMA. 2003;290(22):2985-2991.
212. CDC/NHSN Surveillance Definition of Healthcare-Associated Infection and Criteria for Specific Types of Infections in the Acute Care Setting. Available at https://www.cdph.ca.gov/programs/hai/Documents/Slide-Set-20-Infection-Definitions-NHSN-2013.pdf. Last accessed January 15, 2016.
213. Porzecanski I, Bowton DL. Diagnosis and treatment of ventilator-associated pneumonia. Chest. 2006;130(2):597-604.
214. Miller PR, Johnson JC 3rd, Karchmer T, Hoth JJ, Meredith JW, Chang MC. National nosocomial infection surveillance system: from benchmark to bedside in trauma patients. J Trauma. 2006;60(1):98-103.
215. Zaccard CR, Schell RF, Spiegel CA. Efficacy of bilateral bronchoalveolar lavage for diagnosis of ventilator-associated pneumonia.J Clin Microbiol. 2009;47(9):2918-2924.
216. Berton D, Kalil AC, Teixeira PJ. Quantitative versus qualitative cultures of respiratory secretions for clinical outcomes in patients with ventilator-associated pneumonia. Cochrane Database Syst Rev. 2012;1:CD006482.
217. Berton DC, Kalil AC, Teixeira PJ. Quantitative versus qualitative cultures of respiratory secretions for clinical outcomes in patients with ventilator-associated pneumonia. Cochrane Database Syst Rev. 2014;10:CD006482.
218. Depuydt P, Myny D, Blot S. Nosocomial pneumonia: aetiology, diagnosis and treatment. Curr Opin Pulm Med. 2006;12(3):192-197.
219. Micek ST, Heuring TJ, Hollands JM, Shah RA, Kollef MH. Optimizing antibiotic treatment for ventilator-associated pneumonia. Pharmacotherapy. 2006;26(2):204-213.
220. Rello J, Vidaur L, Sandiumenge A, et al. De-escalation therapy in ventilator-associated pneumonia. Crit Care Med. 2004;32(11):2183-2190.
221. Kaye KS. Antimicrobial de-escalation strategies in hospitalized patients with pneumonia, intra-abdominal infections, and bacteremia. J Hosp Med. 2012;(7 suppl 1):S13-S21.
222. Sligl W, Taylor G, Brindley PG. Five years of nosocomial gram-negative bacteremia in a general intensive care unit: epidemiology, antimicrobial susceptibility patterns, and outcomes. Int J Infect Dis. 2006;10(4):320-325.
223. Kollef MH, Rello J, Cammarata SK, Croos-Dabrera RV, Wunderink RG. Clinical cure and survival in gram-positive ventilator-associated pneumonia: retrospective analysis of two double-blind studies comparing linezolid with vancomycin. Intensive Care Med. 2004;30(3):388-394.
224. Mullins D, Kuznik C, Shaya FT, Obeidat NA, Levine AR, Liu LZ, Wong W. Cost-effectiveness analysis of linezolid compared with vancomycin for the treatment of nosocomial pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Ther. 2006;28(8):1184-1198.
225. Shorr AF, Susla GM, Kollef MH. Linezolid for treatment of ventilator-associated pneumonia: a cost-effective alternative to vancomycin. Crit Care Med. 2004;32(1):137-143.
226. Patel DA, Michel A, Stephens J, Weber B, Petrik C, Charbonneau C. An economic model to compare linezolid and vancomycin for the treatment of confirmed methicillin-resistant Staphylococcus aureus nosocomial pneumonia in Germany. Infect Drug Resist. 2014;7:273-280.
227. Wunderink RG, Mendelson MH, Somero MS, et al. Early microbiological response to linezolid vs vancomycin in ventilator-associated pneumonia due to methicillin-resistant Staphylococcus aureus. Chest. 2008;134(6):1200-1207.
228. Pugh R, Grant C, Cooke RP, Dempsey G. Short-course versus prolonged-course antibiotic therapy for hospital-acquired pneumonia in critically ill adults. Cochrane Database Syst Rev. 2011;10:CD007577.
229. Pugh R, Grant C, Cooke RP, Dempsey G. Short-course versus prolonged-course antibiotic therapy for hospital-acquired pneumonia in critically ill adults. Cochrane Database Syst Rev. 2015;8:CD007577.
230. van Nieuwenhoven CA, Vandenbroucke-Grauls C, van Tiel FH, et al. Feasibility and effects of the semirecumbent position to prevent ventilator-associated pneumonia: a randomized study. Crit Care Med. 2006;34(2):396-402.
231. 231. How-To Guide: Prevent Ventilator-Associated Pneumonia. Cambridge, MA: Institute for Healthcare Improvement; 2012.
232. Jain M, Miller L, Belt D, King D, Berwick DM. Decline in ICU adverse events, nosocomial infections and cost through a quality improvement initiative focusing on teamwork and culture change. Qual Saf Health Care. 2006;15(4):235-239.
233. Stone MJ, Snetman D, O'Neill A, et al. Daily multidisciplinary rounds to implement the ventilator bundle decreases ventilator-associated pneumonia in trauma patients: but does it affect outcome? Surg Infect (Larchmt). 2011;12(5):373-378.
234. Cachecho R, Dobkin E. The application of human engineering interventions reduces ventilator-associated pneumonia in trauma patients. J Trauma Acute Care Surg. 2012;73(4):939-943.
235. Tolentino-DelosReyes AF, Ruppert SD, Shiao S-YPK. Evidence-based practice: use of the ventilator bundle to prevent ventilator-associated pneumonia. Am J Crit Care. 2007;16(1):20-27.
236. Seymann GB, Di Francesco L, Sharpe B, et al. The HCAP gap: differences between self-reported practice patterns and published guidelines for health care-associated pneumonia. Clin Infect Dis. 2009;49(12):1868-1874.
237. Blot SI, Depuydt P, Annemans L, et al. Clinical and economic outcomes in critically ill patients with nosocomial catheter-related bloodstream infections. Clin Infect Dis. 2005;41(11):1591-1598.
238. Hollenbeak CS. The cost of catheter-related bloodstream infections: implications for the value of prevention. J Infus Nurs. 2011;34(5):309-313.
239. Maki DG, Kluger DM, Crnich CJ. The risk of bloodstream infection in adults with different intravascular devices: a systematic review of 200 published prospective studies. Mayo Clin Proc. 2006;81(9):1159-1171.
240. Chaiyakunapruk N, Veenstra DL, Lipsky BA, Saint S. Chlorhexidine compared with povidone-iodine solution for vascular catheter-site care: a meta-analysis. Ann Intern Med. 2002;136(11):792-801.
241. Chaiyakunapruk N, Veenstra DL, Lipsky BA, Sullivan SD, Saint S. Vascular catheter site care: the clinical and economic benefits of chlorhexidine gluconate compared with povidone iodine. Clin Infect Dis. 2003;37(6):764-771.
242. Mermel LA, McCormick RD, Springman SR, Maki DG. The pathogenesis and epidemiology of catheter-related infection with pulmonary artery Swan-Ganz catheters: a prospective study utilizing molecular subtyping. Am J Med. 1991;91(3B):197S-205S.
243. Merrer J, De Jonghe B, Golliot F, et al. Complications of femoral and subclavian venous catheterization in critically ill patients: a randomized controlled trial. JAMA. 2001;286(6):700-707.
244. Deshpande KS, Hatem C, Ulrich HL, et al. The incidence of infectious complications of central venous catheters at the subclavian, internal jugular, and femoral sites in an intensive care unit population. Crit Care Med. 2005;33(1):13-20.
245. Maki DG, Knasinski V, Halvorson K, Tambyah PA. A novel silver-hydrogel-impregnated indwelling urinary catheter reduces CAUTIs: a prospective double-blind trial [abstract]. Infect Control Hosp Epidemiol. 1998;19:682.
246. Darouiche RO, Raad II, Heard SO, et al. A comparison of two antimicrobial-impregnated central venous catheters. N Engl J Med. 1999;340(1):1-8
247. Brun-Buisson C, Doyon F, Sollet JP, Cochard JF, Cohen Y, Nitenberg G. Prevention of intravascular catheter-related infection with newer chlorhexidine-silver sulfadiazine-coated catheters: a randomized controlled trial. Intensive Care Med. 2004;30(5):837-843.
248. Safdar N, Fine JP, Maki DG. Meta-analysis: methods for diagnosing intravascular device-related bloodstream infection. Ann Intern Med. 2005;142(6):451-466.
249. Mermel LA, Allon M, Bouza E, et al. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis. 2009;49(1):1-45.
250. Raad I. Management of intravascular catheter-related infections. J Antimicrob Chemother. 2000;45(3):267-270.
251. Morrell M, Fraser VJ, Kollef MH. Delaying the empiric treatment of Candida bloodstream infection until positive blood culture results are obtained: a potential risk factor for hospital mortality. Antimicrob Agents Chemother. 2005;49(9):3640-3645.
252. Hsu RB. Risk factors for nosocomial infective endocarditis in patients with methicillin-resistant Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol. 2005;26(7):654-657.
253. Krein SL, Hofer TP, Kowalski CP, et al. Use of central venous catheter-related bloodstream infection prevention practices by U.S. hospitals. Mayo Clin Proc. 2007;82(6):672-678.
254. Warren DK, Cosgrove SE, Kiekema DJ, et al. A multicenter intervention to prevent catheter-associated bloodstream infections. Infect Control Hosp Epidemiol. 2006;27(7):662-669.
255. 255. How-to Guide: Prevent Central Line-Associated Bloodstream Infections. Cambridge, MA: Institute for Healthcare Improvement; 2012.
256. Shapey IM, Foster MA, Whitehouse T, et al. Central venous catheter-related bloodstream infections: improving post-insertion catheter care. J Hosp Infect. 2009;71(2):117-122.
257. Guerin K, Wagner J, Rains K, Bessesen M. Reduction in central line-associated bloodstream infections by implementation of a postinsertion care bundle. Am J Infect Control. 2010;38(6):430-433.
258. Warren DK, Yokow DS, Climo MW, et al. Preventing catheter-associated bloodstream infections: a survey of policies for insertion and care of central venous catheters from hospitals in the Prevention Epicenter Program. Infect Cont Hosp Epidemiol. 2006;27(1):8-13.
259. Sunenshine RH, McDonald LC. Clostridium difficile-associated disease: new challenges from an established pathogen. Clev Clin J Med. 2006;73(2):187-197.
260. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from U.S. short-stay hospitals, 1996–2003. Emerging Infect Dis. 2006;12(3):409-415.
261. McDonald LC. Clostridium difficile: responding to a new threat from an old enemy. Infect Cont Hosp Epidemiol. 2005;26(8):672-675.
262. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000–2005. Emerg Infect Dis. 2008;14(6):929-931.
263. Gerding DN, Muto CA, Owens RC Jr. Treatment of Clostridium difficile infection. Clin Infect Dis. 2008;46(Suppl 1):S32-S42.
264. Dubberke ER, Gerding DN, Classen D, Arias KM. Strategies to prevent Clostridium difficile infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29(suppl 1):S81-S92.
265. Dubberke ER, Reske KA, Olsen MA, McDonald LC, Fraser VJ. Short- and long-term attributable cost of Clostridium difficile-associated disease in non-surgical patients. Clin Infect Dis. 2008;46(4):497-504.
266. Song X, Bartlett JG, Speck K, Naegeli A, Carroll K, Perl TM. Rising economic impact of Clostridium difficile-associated disease in adult hospitalized patient population. Infect Control Hosp Epidemiol. 2008;29(9):823-828.
267. Lipp MJ, Nero DC, Callahan MA. Impact of hospital-acquired Clostridium difficile. J Gastroenterol Hepatol. 2012;27(11):1733-1737.
268. Leclair M-A, Allard C, Lesur O, Pépin J. Clostridium difficile infection in the intensive care unit. J Intensive Care Med. 2010;25(1):23-30.
269. Halsey J. Current and future treatment modalities for Clostridium difficile-associated disease. Am J Health Syst Pharm. 2008;65(8):705-715.
270. Pillai A, Nelson R. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database Syst Rev. 2008;(1):CD004611.
271. Haley RW, Quade D, Freeman HE, Bennett JV. Study on the efficacy of nosocomial infection control (SENIC Project): summary of study design. Am J Epidemiol. 1980;111(5):472-485.
272. Haley RW, Culver DH, White JW, et al. The efficacy of infection surveillance and control programs in preventing nosocomial infections in U.S. hospitals. Am J Epidemiol. 1985;121(2):182-205.
273. Association for Professionals in Infection Control and Epidemiology. Infection Prevention and You. Available at http://www.apic.org/Resource_/TinyMceFileManager/IP_and_You/IPandYou_SmallFlyer_download_hiq.pdf. Last accessed January 15, 2016.
274. Kaye KS, Engemann JJ, Fulmer EM, Clark CC, Noga EM, Sexton DJ. Favorable impact of an infection control network on nosocomial infection rates in community hospitals. Infect Control Hosp Epidemiol. 2006;27(3):228-232.
275. Anderson DJ, Miller BA, Chen LF, et al. The network approach for prevention of healthcare-associated infections: long-term effect of participation in the Duke Infection Control Outreach Network. Infect Control Hosp Epidemiol. 2011;32(4):315-322.
276. Erasmus V, Daha TJ, Brug H, et al. Systematic review of studies on compliance with hand hygiene guidelines in hospital care.Infect Control Hosp Epidemiol. 2010;31(3):283-294.
277. Johnson PDR, Rhea M, Burrell LJ, et al. Efficacy of an alcohol/chlorhexidine hand hygiene program in a hospital with high rates of nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection. Med J Aust. 2005;183(10):509-514.
278. Gordin FM, Schultz ME, Huber RA, Gill JA. Reduction in nosocomial transmission of drug-resistant bacteria after introduction of an alcohol-based handrub. Infect Control Hosp Epidemiol. 2005;26(7):650-653.
279. Gould DJ, Moralejo D, Drey N, Chudleigh JH. Interventions to improve hand hygiene compliance in patient care. Cochrane Database Syst Rev. 2010;(9):CD005186.
280. The Joint Commission. Measuring Hand Hygiene Adherence. Overcoming the Challenges. Oakbrook Terrace, IL: The Joint Commission; 2009.
281. Salgado CD, Giannetta ET, Hayden FG, Farr BM. Preventing nosocomial influenza by improving the vaccine acceptance rate of clinicians. Infect Control Hosp Epidemiol. 2004;25(11):923-928.
282. Carman WF, Elder AG, Wallace LA, et al. Effects of influenza vaccination on health-care workers on mortality of elderly people in long-term care: a randomized controlled trial. Lancet. 2000;355(9198):93-97.
283. Centers for Disease Control and Prevention. Recommended Vaccines for Healthcare Workers. Available at http://www.cdc.gov/vaccines/adults/rec-vac/hcw.html. Last accessed January 15, 2016.
284. Pearson ML, Bridges CB, Harper SA. Influenza vaccination of health-care personnel. MMWR. 2006;55(RR02):1-16.
285. Nichol K. Improving influenza vaccination rates among adults. Cleve Clin J Med. 2006;73(11):1009-1015.
286. Centers for Disease Control and Prevention. Influenza Vaccination Information for Health Care Workers. Available at http://www.cdc.gov/flu/healthcareworkers.htm. Last accessed January 15, 2016.
287. Christini AB, Shutt KA, Byers KE. Influenza vaccination rates and motivators among healthcare worker groups. Infect Control Hosp Epidemiol. 2007;28(2):171-177.
288. Dash GP, Fauerbach L, Pfeiffer J, et al. APIC position paper: improving health care worker influenza immunization rates. Am J Infect Control. 2004;32(3):123-125.
289. Institute for Healthcare Improvement. How-to Guide: Reduce MRSA Infection. Available at http://www.ihi.org/resources/Pages/Tools/HowtoGuideReduceMRSAInfection.aspx. Last accessed January 15, 2016.
290. Harbarth S, Fankhauser C, Schrenzel J, et al. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA. 2008;299(10):1149-1157.
291. Robicsek A, Beaumont JL, Paule SM, et al. Universal surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med. 2008;148(6):409-418.
292. Harbarth S, Sax H, Uckay I, et al. A predictive model for identifying surgical patients at risk of methicillin-resistant Staphylococcus aureus carriage on admission. J Am Coll Surg. 2008;207(5):683-689.
293. Raymond DP, Pelletier SJ, Sawyer RG. Antibiotic utilization strategies to limit antimicrobial resistance. Semin Respir Crit Care Med. 2002;23(5):497-501.
294. Wibbenmeyer L, Danks R, Faucher L, et al. Prospective analysis of nosocomial infection rates, antibiotic use, and patterns of resistance in a burn population. J Burn Care Res. 2006;27(2):152-160.
295. Raboud J, Saskin R, Wong K, et al. Patterns of handwashing behavior and visits to patients on a general medical ward of healthcare workers. Infect Control Hosp Epidemiol. 2004;25(3):198-202.
296. Warren DK, Zack JE, Cox MJ, Cohen MM, Fraser VJ. An educational intervention to prevent catheter-associated bloodstream infections in a nonteaching, community medical center. Crit Care Med. 2003;31(7):1959-1963.
297. Coopersmith CM, et al. Effect of an education program on decreasing catheter-related bloodstream infections in the surgical intensive care unit. Crit Care Med. 2002;30(1):59-64.
298. Lee TC, Moore C, Raboud JM, et al. Impact of a mandatory infection control education program on nosocomial acquisition of methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol. 2009;30(3):249-256.
299. Grol R, Grimshaw J. From best evidence to best practice: effective implementation of change in patients' care. Lancet. 2003;362(9391):1225-1230.
300. Pande PS, Neuman RP, Cavanagh RR. The Six Sigma Way: How GE, Motorola, and Other Top Companies are Honing their Performance. New York, NY: McGraw Hill; 2000.
301. Eldridge NE, Woods SS, Bonello RS, et al. Using the Six Sigma process to implement the Centers for Disease Control and Prevention guideline for hand hygiene in 4 intensive care units. J Gen Intern Med. 2006;21(Suppl 2):S35-S42.
302. Hofmann F, Erracin C, Marsh G, Dumas R. Influenza vaccination of healthcare workers: a literature review of attitudes and beliefs. Infection. 2006;34(3):142-147.
303. Hollmeyer HG, Hayden F, Poland G, Buchholz U. Influenza vaccination of health care workers in hospitals: a review of studies on attitudes and predictors. Vaccine. 2009;27(30):3935-3944.
304. Committee on Health Literacy Board on Neuroscience and Behavioral Health. Health Literacy: A Prescription to End Confusion. Washington, DC: The National Academies Press; 2004.
305. Kirsch I, Jungeblut A, Jenkins L, Kolstad A. Adult Literacy in America: A First Look at the Results of the National Adult Literacy Survey (NALS). Washington, DC: National Center for Education Statistics, U.S. Department of Education; 1993.
306. U.S. Census Bureau. Selected Social Characteristics in the United States: 2014. Available at http://factfinder.census.gov/faces/tableservices/jsf/pages/productview.xhtml?pid=ACS_14_5YR_DP02&src=pt. Last accessed January 15, 2016.
307. Sevilla Matir J, Willis DR. Using bilingual staff members as interpreters. Fam Pract Manag. 2004;11(7):34-36.
308. Ngo-Metzger Q, Massagli MP, Clarridge BR, et al. Linguistic and cultural barriers to care: perspectives of Chinese and Vietnamese immigrants. J Gen Intern Med. 2003;18(1):44-52.
309. Flores G. Language barriers to health care in the United States. N Engl J Med. 2006;355(3):229-231.
310. Flores G. The impact of medical interpreter services on the quality of health care: a systematic review. Med Care Res Rev. 2005;62(3):255-299.
311. Karliner L, Jacobs EA, Chen AH, Mutha S. Do professional interpreters improve clinical care for patients with limited English proficiency? A systematic review of the literature. Health Serv Res. 2007;42(2):727-754.
312. Centers for Disease Control and Prevention. Steps of An Outbreak Investigation. Available at http://www.cdc.gov/ophss/csels/dsepd/ss1978/lesson6/section2.html. Last accessed January 15, 2016.
313. Centers for Disease Control and Prevention. Infection Prevention and Control Recommendations for Hospitalized Patients Under Investigation (PUIs) for Ebola Virus Disease (EVD) in U.S. Hospitals. Available at http://www.cdc.gov/vhf/ebola/healthcare-us/hospitals/infection-control.html. Last accessed January 15, 2016.
314. Gastmeier P, Stamm-Balderjahn S, Hansen S, Nitzschke-Tiemann F, Zuschneid I, Groneberg K, Ruden H. How outbreaks can contribute to prevention of nosocomial infection: analysis of 1,022 outbreaks. Infect Cont Hosp Epidemiol. 2005;26(4):357-361.
315. Breathnach AS, Riley PA, Shad S, Jownally SM, Law R, Chin PC, Kaufmann ME, Smith EJ. An outbreak of wound infection in cardiac surgery patients caused by Enterobacter cloacae arising from cardioplegia ice. J Hosp Infect. 2006;64(2):124-128.
316. Felkner M, Pascoe N, Shupe-Ricksecker K, Goodman E. The wound care team: a new source of group A streptococcal nosocomial transmission. Infect Control Hosp Epidemiol. 2005;26(5):462-465.
317. Jensen PA, Lambert LA, Iademarco MF, Ridzon R. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care settings, 2005. MMWR. 2005;54(RR17):1-141.
318. Henderson DK. Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. Am J Med. 2006;119(6 Suppl 1):S45-S52, S62-S70.
319. Spellberg B. New Antibiotic Development: Barriers and Opportunities in 2012. Available at http://www.tufts.edu/med/apua/news/news-newsletter-vol-30-no-1-2.shtml. Last accessed January 20, 2016.
320. Centers for Disease Control and Prevention. Get Smart for Healthcare. Available at http://www.cdc.gov/getsmart/healthcare/. Last accessed January 20, 2016.
1. Hooton TM, Bradley SF, Cardenas DD, et al. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis. 2010;50(5):625-663. Summary retrieved from National Guideline Clearinghouse at http://www.guideline.gov/content.aspx?id=24060. Last accessed January 17, 2013.
2. Card R, Sawyer M, Degnan B, et al. Perioperative Protocol: Health Care Protocol. Bloomington, MN: Institute for Clinical Systems Improvement; 2014. Summary retrieved from National Guideline Clearinghouse at http://www.guideline.gov/content.aspx?id=48408. Last accessed January 28, 2016.
3. Institute for Clinical Systems Improvement. Prevention of Ventilator-Associated Pneumonia: Health Care Protocol. Bloomington, MN: Institute for Clinical Systems Improvement; 2011. Summary retrieved from National Guideline Clearinghouse at http://www.guideline.gov/content.aspx?id=36063. Last accessed January 28, 2016.
4. O'Grady NP, Alexander M, Burns LA, et al. Guidelines for the Prevention of Intravascular Catheter-Related Infections, 2011. Atlanta, GA: Centers for Disease Control and Prevention; 2011. Summary retrieved from National Guideline Clearinghouse at http://www.guidelines.gov/content.aspx?id=34426. Last accessed January 28, 2016.
5. Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431-455. Summary retrieved from National Guideline Clearinghouse at http://www.guideline.gov/content.aspx?id=15952. Last accessed January 28, 2016.
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