EvidenceBased Infection Control In Clinical Practice: If You Buy ...

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Review J Vet Intern Med 2013;27:430–438

Evidence-Based Infection Control In Clinical Practice: If You Buy Clothes for the Emperor, Will He Wear Them? P.S. Morley In the fabled story of the Emperor’s New Clothes, nakedness is ignored, denied, and accepted despite its obviousness. Similarly, we seemingly have ignored, denied, and accepted the risks of healthcare-associated infections (HCAI) in veterinary settings, despite common occurrence and obvious importance. Risks for HCAI in veterinary medicine cannot be denied and are increasingly apparent because of improved surveillance and reporting. We have an ethical responsibility to take all reasonable precautions to minimize foreseeable infectious disease hazards, and provide an environment in which personnel and patients are protected from infectious disease hazards so that care can be optimized. Yet, there is often a pronounced mismatch between what we know about risks for infectious disease and our actions. Veterinarians often fail to act on well-known, universally accepted risks for infectious disease in patients and in people contacting these animals. We must educate personnel so they are well-versed regarding agents commonly causing HCAI (including zoonotic infections), can identify patients with higher risks for shedding agents and for developing HCAI, have awareness of which procedures and management practices are associated with higher rates of HCAI, and have skill in applying effective prevention methods. We need to develop standardized benchmarks for risks of HCAI in veterinary settings, better understand efficacy and cost-effectiveness for prevention practices, and develop good educational materials that will promote an effective understanding of risks and prevention methods for HCAI among personnel and the public. We need to buy new clothes for the emperor and be sure he actually wears them! Key words: Biosecurity; Nosocomial infection; Healthcare-associated infections; Zoonosis; Ethics; Calvin Schwabe.

he overarching goal of infection control in health care settings is to provide an environment in which personnel and patients are protected from infectious disease hazards so that care can be optimized.1 Although infection control is not the sole or primary focus of patient care, the full potential of our health care efforts cannot be realized unless appropriate methods are used to prevent infectious diseases that can harm patients. In other words, excellent patient care can never be achieved unless we control risks for healthcare-associated infections (HCAI). Adverse outcomes related to HCAI are a well-recognized threat in human and veterinary medicine.1–3 Despite the similarities between care available in human and veterinary health care facilities, and the long-standing pattern of veterinary care benefiting from advancements developed for use in human patients, infection control efforts in veterinary hospitals generally lack the organized attention that they receive in modern human health care facilities. In fact, infection control efforts can be quite rudimentary in

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From the department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, James L. Voss Veterinary Teaching Hospital, Fort Collins, CO. This paper was presented as part of the 2011 Calvin W. Schwabe Symposium honoring Dr Dale D. Hancock for lifetime achievement in veterinary epidemiology and preventive medicine, sponsored by the Association for Veterinary Epidemiology and Preventive Medicine, December 2011, Chicago, IL. Corresponding author: Paul S. Morley, DVM, PhD, DACVIM, Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, James L. Voss Veterinary Teaching Hospital, Colorado State University, Fort Collins, CO 80523-1678, e-mail: [email protected]

Submitted December 7, 2012; Revised January 7, 2013; Accepted January 22, 2013. Copyright © 2013 by the American College of Veterinary Internal Medicine 10.1111/jvim.12060

Abbreviations: AVMA CDC CSU HCAI ICU MRSA MRSP OR VTH

American Veterinary Medical Association U.S. Centers for Disease Control and Prevention Colorado State University healthcare-associated infections Intensive Care Unit methicillin-resistant Staphylococcus aureus methicillin-resistant Staphylococcus pseudintermedius odds ratio Veterinary Teaching Hospital

veterinary hospitals, and veterinary personnel frequently are unaware of the advanced approaches that are routinely used to systematically improve infection prevention efforts in human hospitals. These deficits can be further exacerbated by failure of veterinary care-givers to act on first principles in response to well-known risks for HCAI. This review will consider the actions and attitudes of veterinary personnel and the public and the apparent incongruity between our behavior and available information about the risks for HCAI.

Obligations Regarding Prevention of Infections in Health Care Settings Clearly, health care providers have ethical and legal responsibilities to minimize risks for infectious disease transmission in health care settings. The ethical responsibilities regarding infection control for human patients have received increasing attention in the past decade.3–7 Some of this increased attention has been driven by efforts of the U.S. Centers for Disease Control and Prevention (CDC) during the past 40 years to gather and report standardized information about HCAI rates, and by other groups that have established and revised guidelines for best-practice prevention efforts.8 The

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discussion has been further invigorated by implementation of policies from Medicare and other third-party insurers to reduce reimbursement when health of patients has been compromised because of HCAI.3, 9. Unfortunately, there has been little published discussion of the ethical responsibilities regarding HCAI in veterinary settings. Recently, an international group of experts gathered to develop consensus opinions about the future of infection control in equine populations.10 A unanimous conclusion from the group was that veterinarians and managers of animal populations need to be universally aware that there is a recognizable standard of care regarding infection control. Failure to meet this standard constitutes malpractice and represents a failure to meet our minimum ethical responsibilities to patients and clients. Part of this standard of care is manifested in the requirement to take all reasonable precautions to minimize foreseeable infectious disease hazards for our personnel, and to educate clients and other members of the public about the real hazards related to zoonotic disease exposure. Whether we are functioning as students, as technicians or nursing staff, as graduate veterinarians, or perhaps especially as veterinary specialists, it is tempting to take each patient as an individual without considering that they belong to the larger population of current and future patients. It is tempting to believe, especially in tertiary care facilities, that we achieve optimal patient management for a hospital by exhaustively managing every possible need of individual patients without considering the impact on other patients. For example, we might want to provide the most advanced diagnostic evaluations for a severely ill dog with an acute abdomen (eg, physical exams by multiple specialists, ultrasound and radiographic exams, endoscopy), moving the patient from room to room throughout a day in a large hospital only to later receive laboratory confirmation of parvovirus infection. Similarly, a whole host of personnel and equipment can be used in delivering state-of-the-art intensive care to critically ill foals or adult horses with severe ataxia, only to later learn that this intensive management has facilitated contamination of the hospital environment and spread of contagious agents to other patients. Thus, by intensively focusing on the care of one patient we can decrease the quality of care we provide for other patients by affecting the potential for HCAI. In each patient care decision we must be concerned about whether the actions used in managing today’s patients will create increased risk for patients that enter the hospital tomorrow.

Documented Risks for HCAI Data available in the United States suggest that on average approximately 4.5% of human patients experience HCAI every year, and there are approximately 9.3 HCAI per 1,000 patient-hospitalization-days.11 Risks of infection vary substantially among different patient types, with highest rates occurring in the most critically ill patients and those undergoing more invasive interventions. It has been estimated that approxi-

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mately 30% of intensive care unit (ICU) patients in higher-income countries develop some type of HCAI.12 Based upon the systematic collection of data through the National Nosocomial Infections Surveillance system, it was estimated that in 2002 approximately 1.7 million HCAI occurred in human hospitals in the United States that participated in surveillance sponsored by the CDC, and these infections caused or were associated with death during hospitalization in approximately 5.8% (99,000/1.7 million) of these patients (this does not include deaths that occurred after discharge that were attributable to HCAI).11 The annual economic impact of HCAI in the U.S. health care system in 2004 was estimated to be approximately US$28-$45 billion.3,13 For perspective, these HCAI exceeded the number of cases of every notifiable infectious disease in the United States, and deaths associated with HCAI rank among the top 10 causes of death reported in the United States The increased costs attributable to HCAI provide an idea of the potential savings that might be achieved by preventing all HCAI, but these estimates must be considered relative to the cost and efficacy of prevention programs that might be employed. It is generally held true that not all HCAI are preventable, and estimates of the preventable fraction vary substantially depending on the type of infection and the magnitude or extent of preventive measures that can be employed. In 1 systematic review regarding the preventable fraction of HCAI, the authors found that the estimated impact of prevention programs varied from 10% reduction in HCAI to 70%,14 but some of this variability likely was attributable to the use of different surveillance methods and different definitions for HCAI. The authors concluded that the greatest reduction potential was likely related to central-line-associated blood stream infections (up to 70% preventable fraction), and was notably lower with surgical site infections and other types of HCAI. Overall, the authors concluded that at least 20% of all HCAI likely are preventable using current medical practices and technology. Assuming that 20% of all HCAI were prevented, this would be accompanied by an estimated benefit of US$5.7-$9.0 billion compared to a benefit of US$14.2-$22.5 billion if 50% of HCAI were prevented.13. Unfortunately, we do not have systems in place to obtain similar information about endemic infection rates from standardized surveillance systems in veterinary care facilities. Some veterinary hospitals engage in pathogen-specific surveillance (eg, Salmonella or methicillinresistant Staphylococcus aureus [MRSA]) using actively or passively collected laboratory data,15 but efforts to characterize the occurrence of clinical disease (as opposed to recovery of specific agents) through surveillance are very rare. One study used active syndromic surveillance to estimate the rates of occurrence for 7 clinical syndromes in equine and small animal critical care patients.16,17 Overall, it was estimated that  1 nosocomial disease syndromes developed in approximately 16% of ICU patients and there were approximately 4.3 events per 100 patient-days of hospitalization.

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More information is available about epidemics of HCAI in veterinary patients than there is regarding endemic HCAI rates. In fact, most published information about HCAI in veterinary hospitals comes from reports of outbreaks related to a variety of infectious agents.18–34 These reports suggest that outbreaks of HCAI are a common hazard in veterinary hospitals. This is corroborated by a survey of veterinary teaching hospitals in which 82% (31/38) reported identifying outbreaks of HCAI in the 5 years preceding the survey, and 45% (17/38) detected >1 outbreak in this same period.15 The 2 most common causes of these reported outbreaks were Salmonella (65%, 20/31) and MRSA (42%, 13/31), both of which are frequently recognized in association with zoonotic infections in veterinary care settings. Fifty-eight percent (22/38) of these facilities restricted admissions as part of the efforts to control outbreaks, and 12 of 38 equine hospitals temporarily closed in order to clean the hospital environment and mitigate risks for patients. Administrators of hospitals participating in this survey identified 50 people as being the most knowledgeable individuals in their facilities about infection control.15 Seventy-eight percent (39/50) of these experts reported they had greater or much greater awareness or concern about HCAI at the time of interviews in comparison to 10 years before the survey. Sixty-four percent reported that this increased concern about HCAI was accompanied by greater true risk of infection for their patients during the same period. This is perhaps not surprising given the increased availability of intensive management of veterinary patients of all types. The increased risk for death among patients with HCAI is well documented in humans, particularly those who are critically ill.11–13,35,36 There is notable corroboration from outbreaks of HCAI that have been described in veterinary hospitals, although the full scope of outbreaks in veterinary settings frequently has not been recognized or investigated. This is clearly evident in reported outbreaks of nosocomial Salmonellosis where as many as 30-60% of affected animals have died as a result of HCAI,27,30–32 but it is also evident with other types of HCAI.26,33,34,37 Closure of hospitals or restriction of activities frequently is necessary to ensure patient safety and mitigate these outbreaks. The authors of 1 report made a notable conclusion about the impact of the outbreak saying that “closure of the VTH affected all missions of the institution and had substantial financial impact (US$4.12 million).”27 These reports are remarkable in their scale, severity of clinical disease, substantial detrimental impact on patients, and tremendous impact on the hospitals. However, it is also notable that many of these reported outbreaks occurred at tertiary care facilities that are world renowned for their excellence in patient care. Thus, we should not conclude HCAI or the related deaths described in these reports occurred because patient care at these hospitals was worse than average, but rather that the case fatality likely could have been worse at other veterinary facilities. Furthermore,

comparing the large number of veterinary hospitals that reported having identified outbreaks15 to the limited number of case reports documenting these epidemics suggests that the examples noted above are possibly representative of what is happening regularly rather than being remarkable exceptions to the norm. Many of the agents most commonly causing nosocomial disease outbreaks in veterinary hospitals are zoonotic agents,15 and it is relatively common for human illness to be recognized during these outbreaks even if the attack rates for zoonotic infections often are considered to be low. Unfortunately, there is generally less information available about risks to personnel than there is regarding the risks to patients. Some outbreaks that have been objectively investigated to identify human infection and illness suggest that attack rates in people exposed during these epidemics actually can be quite high (eg, 25-50%) during outbreaks of HCAI in veterinary facilities.23,24,38,39 In the survey reported by Benedict et al,15 systematic surveillance efforts were not routinely used to identify zoonotic disease among humans in the participating veterinary hospitals. Despite this, 50% (19/38) of veterinary teaching hospitals still reportedly identified important clinical disease related to zoonotic infections among personnel in the 2 years before to the interviews.15 Unfortunately, it is clear that owners can also become infected and develop clinical disease because of infections that their animals acquire in veterinary hospitals.23,24,39 Perhaps worst of all, these reports substantiate the idea that many people with high risks for exposure are especially susceptible (eg, the very young and the elderly), and that these zoonotic infections can result in life-threatening illness as shown by the need for hospitalization in some cases. It is also notable that several of these documented zoonotic infections resulted from exposure to small animal patients.24,39,40 Personal experience in consulting with veterinarians about infection control suggests that these are not rare risks, but rather that occurrences generally have not been reported in the scientific literature.

How Do We Respond to These Challenges? Experience working and consulting on infection control in veterinary hospitals leads me to conclude that there is often a pronounced mismatch between what we know about the risks for infectious disease and our actions. Despite the well-known and well-documented risks for HCAI in human hospitals, the frequent reports of outbreaks of HCAI in veterinary hospitals, the increase in awareness about HCAI, the perceived increase in risks related to HCAI in veterinary settings, and the important consequences of these infections, veterinarians and veterinary personnel often fail to routinely act to mitigate these risks. We know about these hazards and yet we act incongruously. For example, we know that hand washing is a simple yet effective method for protecting ourselves and our patients. This is nicely illustrated by Anderson et al,41 who found that veterinary personnel had only one-third of the risk for

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MRSA nasal colonization (odds ratio [OR] = 0.27), if they reported washing hands after handling horses thought to have infectious diseases, or washing their hands between visiting different equine farms (OR = 0.35). However, in a survey of members of the American Veterinary Medical Association (AVMA), only 18% of large animal veterinarians and 48% of small animal veterinarians reported that they always washed hands or used other hand hygiene practices between patient contacts.42. Part of the problem likely is that we think we are doing a better job in controlling HCAI than we actually are. When asked about the effectiveness of infection control practices used at veterinary teaching hospitals at AVMA-accredited institutions, 86% (43/ 50) of infection control specialists believed there were substantial differences among hospitals.15 Forty-two percent (21/50) of these people also reported that they had rigorous infection control programs at their hospitals, and 40% reported that their veterinary teaching hospital ranked in the top 10% of peer institutions in terms of the rigor and effectiveness of their infection control programs. Clearly 40% of institutions cannot be ranked in the top 10%, which raises the question of whether a false sense of adequacy could lead to complacency. There also is an apparent tendency to recognize that problems with HCAI can occur, but to believe that these problems are more likely to happen to other people or in other hospitals. For example, in a survey of veterinarians regarding attitudes about antimicrobial resistance, 63% of respondents considered veterinary prescribing practices to be an important or very important factor contributing to development of antimicrobial resistance when discussing use in companion animals or horses. Similarly, 84% of respondents considered prescribing practices to be important or very important when discussing use in food animals.43,44 However, only 1% of participating veterinarians said that their own prescribing practices frequently led to the development of resistant bacteria, and 90% said that their prescribing practices never or rarely did. There also is an apparent mismatch between our greatest concerns and the things that are most likely to harm people or our patients in veterinary care environments. Veterinary personnel who commonly manage high risk patients or work in hazardous situations can sometimes underestimate the importance or develop cavalier attitudes regarding commonly encountered hazards. For example, in a survey of personnel working at a large referral veterinary hospital, participants reported that the most common types of occupational related injury, illness, or “near miss” that they had experienced while working in veterinary medicine were related to physical hazards, such as animal-related injuries (eg, bites, kicks, scratches, crush injuries) or other physical injuries such as those experienced while lifting or moving heavy objects.45 These physical injuries or near misses were 5 to 6 times more commonly reported than events related to biological hazards, and >10 times more commonly reported than events related

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to chemical hazards. However, in the same interview, these participants reported that their concerns regarding occupational injury or illness were much greater for chemical hazards than for infectious disease hazards, and were least for injuries related to physical hazards. Even when we recognize important infection control hazards we often respond inconsistently or paradoxically. One of the most common reasons that clinical personnel at the Colorado State University Veterinary Teaching Hospital (CSU-VTH) consult with Infection Control Personnel is because of concerns about MRSA and methicillin-resistant Staphylococcus pseudintermedius (MRSP). However, many of the initial reactions to these common infectious agents, even among highly trained specialists, can often be characterized as hysterical rather than logical or well-reasoned, especially when there are concerns about zoonotic disease risks. At the same time, despite the high level of concern that seems common in these staff, we routinely see the same people placing themselves at increased risk for exposure and infection by eating and drinking in animal handling areas or failing to use best practices for hand hygiene. Similarly, in a mail survey of veterinary practitioners regarding infection control practices, only 14% of participating small animal veterinarians, 17% of equine practitioners, and 21% of other large animal veterinarians said that they never ate in animal handling areas.42 In the same survey, veterinarians were asked which zoonotic diseases concerned them, and also were asked about precautions that were taken when managing patients. Despite stated concerns, large numbers of respondents who listed dermatophytosis, rabies virus, or gastrointestinal bacterial pathogens did not report using appropriate protective precautions when examining animals with skin disease, neurological disease, or gastrointestinal disease, respectively. Not only are there apparent failures to act on known hazards to protect ourselves and our patients, we also fail to rigorously act in promoting appropriate actions from others. In the survey of veterinary teaching hospitals conducted by Benedict et al (2008), despite recognized outbreaks of HCAI in patients, the occurrence of substantial human illness, and experts’ perceived increase in risk for HCAI, only 42% (16/38) of hospitals required any personnel (eg, faculty, staff, students) to complete any type of training program regarding infection control. This is despite the fact that personnel working with animals can have very limited knowledge about contagious and zoonotic diseases. When workers at randomly selected animal shelters in the western United States were asked questions about 5 important zoonotic diseases or agents (plague, leptospirosis, MRSA, rabies, internal parasites), they were only able to answer an average of 59% of questions correctly regarding the susceptible species, clinical signs of infection, routes of transmission in animals, and routes of transmission to humans. Participants correctly answered an average of 51% of questions about routes of transmission to humans.46

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We are also inconsistent or ineffective in our communication with clients about risks for HCAI as evidenced by the fact that only 37% (14/38) of institutions included statements about risks related to HCAI in informed consent statements that clients signed.15 In a survey of veterinarians from Seattle, WA and the surrounding area, 43% (153/356) of respondents indicated that they had no educational materials for clients available in their practices regarding zoonotic diseases despite the fact that 77% (280/356) reported that it was very important to educate clients about zoonosis prevention.47 Among human patients who were asked to complete a survey about pet contact and zoonoses while visiting their doctor’s office, only 36% of pet owners reported ever receiving information from any source about zoonotic diseases they could acquire from pets or prevention practices for these diseases.48. There is even information suggesting that we feel uncomfortable or inadequate in dealing with clients’ questions about zoonotic diseases, or that perhaps we do not see doing so as our responsibility. In a survey of Connecticut health professionals about zoonotic diseases and public education, only 45% of veterinarians and 6% of pediatricians reported being very comfortable about advising clients or patients about zoonotic diseases.49 When participants were asked to rank health professions in terms of their responsibility to educate the general public about zoonosis prevention, veterinarians ranked physicians highest followed by public health professionals, whereas pediatricians ranked public health officers as having the highest responsibility followed by veterinarians. In other words, we generally believe it is someone else who should deal with these issues! Veterinarians generally are better prepared to provide education regarding zoonotic diseases than are physicians.50 Although caution must be used because veterinary professionals are not licensed to provide medical advice to people, we still can do a better job of fulfilling our public health obligations by educating our clients and the public about risks and methods for preventing zoonotic diseases. The attitudes and knowledge that our clients and other members of the public have regarding infectious diseases are additional factors affecting this challenge. Animal owners often have as many misconceived ideas as credible information about zoonotic diseases, and the internet and media sources often are the primary sources that people use as basis for their understanding. In a survey of U.S. households in 2001, 40% of respondents with internet access reported that they used the internet to obtain information about health care matters.51 Veterinarians should be active in educating the public about important causes of HCAI in animals, especially when the diseases are zoonotic. In a systematic review regarding the public’s knowledge about HCAI in human hospitals, along with sources of information and perceptions about risks related to HCAI, Gould et al reported that the most frequent source of information that people relied upon was the

media. Furthermore, they concluded that lay people have limited access to credible sources of information about HCAI, or if they do, they often are unable to understand the messages from these sources.52 In a study of media stories on MRSA that were published in the UK from 1990 to 2004, 60% of the sources of information that were cited were members of the public and politicians rather than content experts.53 Comparing the information reported and the cited sources, the authors concluded that scientific studies (even the most highly cited articles) had little impact on coverage in newspapers. The way in which news stories can be embellished to draw attention increases the importance of having credible sources of information. In a study intended to summarize how MRSA had been characterized in media published in the UK, the authors reported that MRSA was typically represented as a “lethal ‘superbug’” and articles typically were constructed around an “it could be you” scenario as opposed to a balanced portrayal of risks and prevention strategies.54. The same type of incongruity frequently can be seen between the public’s concerns and actions. Despite concerns about infectious diseases, people routinely engage in behavior that increases the risk for infectious and zoonotic diseases. In the latest in a series of studies sponsored by the American Society for Microbiology and the American Cleaning Institute that evaluated trends in attitudes and behaviors about hand washing, only 42% of U.S. participants said that they always wash their hands after petting a dog or cat, 77% before handling or eating foods, 82% after changing a diaper, and 89% after using the bathroom at home.55 However, these self-reported practices are likely overestimated as the same survey found that 96% of adults say they always wash their hands after using public restrooms but only 85% of people actually were observed to wash their hands in selected public venues. Despite the known increased risk for disease among children for disease related to enterotoxigenic strains of E. coli (e.g., O157:H7) and other common enteric pathogens, and the obvious public concern regarding foodborne exposures to these agents, petting zoos and other venues promoting physical interactions with animals remain popular attractions for children and their parents. These interactions clearly carry systematic risks for health as there are also numerous reports of enteric disease outbreaks in children and adults associated with these public attractions.56–59 In 1 study monitoring behavior of attendees at a petting zoo, the potential health risks were documented by positive environmental cultures that yielded Salmonella from 63% of samples and E. coli O157:H7 from 6%.60 Seventy-four percent of attendees were observed to have had hand contact with animals, 87% had contact with surfaces in animal holding areas, 49% had hand-to-face contact, and 22% ate or drank in animal holding areas. Despite these potential risks, only 38% percent of adults and children used hand hygiene products upon leaving the petting zoo. Similarly, only 58% of attendees were

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observed to use hand hygiene practices after animal contact in a petting zoo in Ontario.61 The pervasiveness of actions that are contrary to perceived and known risks among the general public may explain why similar attitudes and actions extend into the behavior of veterinary personnel. It also demonstrates the need for veterinarians to model best practice behaviors to clients and staff, as well as the need for veterinary personnel to be a source of reliable information about the risks and prevention methods for zoonotic diseases.

Can We Change This Pattern? Veterinary infection control specialists agree that the first step in reducing HCAI in veterinary care settings is developing an awareness among all veterinary personnel for the risks related to nosocomial and zoonotic infections, and that they learn to identify and address hazards predisposing to HCAI in veterinary care settings.10 We have an ethical responsibility to establish effective infection control procedures in all veterinary care facilities,10 and there are several published references outlining approaches for developing robust, comprehensive infection control programs in veterinary facilities.1,62 However, awareness about HCAI and our responses must not be based solely on first principles in response to theoretical threats. Our actions must also be tailored to evidence of disease threats that is documented by surveillance efforts in each setting and must be enacted in the context of the specific environments in which we work. Frequently, veterinarians and other personnel assume that HCAI rarely or never occur in their patients but they also fail to actually look for these problems. In these circumstances, nosocomial events must be so serious or outbreaks so large that they cannot be missed or ignored in the course of patient care activities. Systematic surveillance efforts in human hospitals in the United States and elsewhere have led to profession-wide improvement in recognition and prevention of HCAI in human care settings.2,8 Standardized protocols can be established to aid in control of HCAI without any type of surveillance, but we will fail in opportunities to respond to specific situations or to make systematic improvements if we do not try to identify and document occurrences of HCAI. Even in hospitals with well-established infection control programs, HCAI can be missed without systematic use of surveillance. For example, despite the ongoing use of 2 systems of passive surveillance for MRSA at the CSU-VTH, a cluster of nosocomial MRSA infections with clinical disease was missed until a retrospective investigation was performed as part of a multicenter research effort.63 Although several factors influenced the occurrence of these HCAI, followup epidemiological investigation suggested that 1 particular health care worker was intensively involved with caring for all of the cases. Earlier recognition of this case cluster may have allowed prevention of infections in the latter cases, and also may have mitigated

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health implications of the potential zoonotic infection of the health care worker. Not every HCAI in patients or health care workers is preventable. However, we have an ethical responsibility to take all reasonable precautions to prevent foreseeable hazards for our patients and personnel. How do we approach this task? We need to work to recognize the infection risks for our patients and personnel. These should be considered from the perspective of the usual, daily risks, and we must develop a good appreciation of what constitutes an exceptional risk. We must then work to mitigate daily risks through established infection prevention procedures that are systematically enacted for all patients and health care workers. Success in these efforts is not determined by which particular prevention efforts are used as there can be many roads to the same destination. We can only truly determine the success of our efforts by assessing outcomes (ie, monitoring rates of diseases, clinical syndromes, and infections). Using benchmarks of what the average or acceptable maximal rates of occurrence, we must then respond to exceptional risk situations by use of additional control measures, continuing to increase the rigor of our prevention methods until we are convinced we have adequately protected our patients and personnel and returned infection risks to baseline levels. It seems clear from the incongruity of our actions in the face of well-known risks for HCAI that we need to improve the education of our personnel so that they are well versed regarding which agents commonly cause HCAI (including zoonotic infections), which patients have higher risks for shedding these agents, which patients have higher risks for developing HCAI, which procedures and management practices are associated with higher rates of HCAI, and the methods that can be used to effectively prevent HCAI. These should be enacted throughout the training of veterinary students and technical staff, but must also be reinforced regularly (both formally and by modeling best practice behaviors) on the clinic floor. We also need to develop effective educational tools for the public regarding HCAI in veterinary care settings and methods that should be used to prevent zoonotic infections in their home environments. Some of these messages are nuanced, and must be carefully crafted so as to appropriately disclose risks and provide useful information about prevention, and yet must not exacerbate problems because the information creates inappropriate alarm. Regardless, we must be more rigorous in ensuring that we routinely disclose risks for HCAI to our clients and personnel, both in average risk situations and especially when risks are increased as evidenced by the occurrence of HCAI that are detected in our surveillance efforts. As summarized by Babcock et al,51 “Recognition by the public that infectious disease outbreaks in people can often be attributed to animal contact reinforces the need to educate veterinarians on zoonotic diseases, the role veterinarians play in preventing zoonoses, and the legal liabilities associated with these roles and responsibilities.”

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Conclusions 64

In the fabled story of the Emperor’s New Clothes, his majesty’s nakedness is ignored, denied, and accepted despite its obviousness. Similarly, it seems that all too often we have ignored, denied, and accepted risks for HCAI in veterinary settings, both for our patients and for people, despite their obviousness. The risks for HCAI in veterinary care settings cannot be denied and are becoming increasingly apparent because of improved awareness, surveillance, and reporting. There are clear examples where we have made major advances in improving infection control efforts in veterinary medicine during the past 2 decades, and the profession should applaud and thank the individuals and institutions that have openly shared their experiences with HCAI so that the profession can learn from their efforts. This spirit of collaboration needs to be embraced as we move forward and we need to look for ways to achieve the same success in prevention efforts that has been achieved in human health care setting during the past 40 years.2,8,13 In many circumstances, it will not be possible to directly apply the same methods that have been used in human hospitals, and so we must develop our own approach when necessary. We need to develop a common standardized benchmark for expected baseline risks for HCAI in veterinary care settings and demonstrate how these can be routinely quantified. We need to work to improve our understanding of the efficacy and cost-effectiveness of prevention practices. We need to collaborate to develop good educational materials and standard messages that can be used to promote an effective understanding of risks and prevention methods for HCAI for veterinary personnel and the public. In a sense, we need to buy new clothes for the emperor. If we do this, however, we also need to make sure that we are no longer denying the obvious. We need to make sure that the emperor actually wears the new clothes! Veterinarians routinely fail to act on well-known, universally accepted risks for infectious disease in their patients and in people contacting these animals. The question remains, are we willing to be average, or do we want to be exceptional?

Acknowledgments The author acknowledges the Biosecurity House Officers, other personnel from the CSU-VTH, and colleagues working on infection control in other hospitals who have helped in the development of the personal philosophy expressed in this manuscript. Conflict of Interest: Author discloses no conflict of interest.

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