Infection Control Practices Employed Within Small Animal Veterinary Practices - a Systematic Review

DR. ANGELA NATALIE WILLEMSEN (Orcid ID : 0000-0003-2198-9500)

Article type : Review

Corresponding author mail id:- [email protected]

Infection control practices employed within small animal veterinary practices - A systematic review

Infection control in veterinary practices Angela Willemsen1, Rowland Cobbold2, Justine Gibson2, Kathryn Wilks3, Sheleigh Lawler1, Simon Reid1

1The University of Queensland, School of Public Health, Herston, Queensland, Australia 21The University of Queensland, School of Veterinary Science, Gatton, Australia

3 Infectious Diseases and Medical Microbiology, Sunshine Coast University Hospital, Birtinya, Queensland, Australia

Acknowledgements

I am grateful to the authors of the literature included in this review who responded to requests for additional information.

This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/ZPH.12589

Background Effective infection control (IC) provides a safe environment for staff, clients and animals of veterinary practices by reducing the risk of nosocomial and zoonotic infections, which are associated with increased hospital stays, costs, morbidity and mortality. An equally important issue arising from nosocomial infection is the loss of trust between the client and the veterinary practice that has potential negative impacts on the veterinary practice in terms of economic risk and the wellbeing of staff. Furthermore, an emerging and significant threat, in this context, is antimicrobial resistance.

The aim of this systematic review was to critically review published reports that documented current IC practices and evaluated interventions to improve IC practices.

Methods A systematic literature search using ten databases to identify papers published over a 20 year period (February 1996 to February 2016) was conducted for studies that met the inclusion criteria. Included studies were assessed using the PRISMA and STROBE-Vet statements.

Results and Discussion A total of 14 of 1615 identified studies met our inclusion criteria. Infection control practices included; hand hygiene, sharps handling, environmental cleaning, personal protective equipment and personnel vaccination. Descriptive studies were the predominant research design for assessing IC compliance. Only three studies were interventions. Compliance with IC protocols was poor and only marginally increased with multi-modal educational campaigns.

There was significant variation in the implementation of IC by veterinary staff. Workplaces that had IC policies, management support and a staff member supporting their implementation were more likely to embrace good IC. Infection control data in veterinary practices was inconsistently reported and collected.

Clearly defining IC and determining prevalence of these practices within the veterinary field is important given the limited research in this area. Further, developing and implementing educational campaigns for this sector is needed.

Keywords

Companion / small animals Hand hygiene

Impacts

 Infection control within small veterinary practices is an important way of minimising the risk of nosocomial (hospital acquired) infections and zoonotic diseases.  Employing adequate infection control practices will reduce the need for antimicrobial use, which contributes to the reduction of antimicrobial resistance, an issue in animal and human health.  The included studies suggest that strategies such as adequate management support, appropriate policy documents and a dedicated staff member monitoring and implementing recommended practices may improve IC practices.

Introduction

The aim of Infection control (IC) is to reduce the risk of transmission of pathogens by disrupting access to either the source, transmission mode or the host, in human and animal health contexts. It includes practices such as hand hygiene, disinfection, sharps management, vaccination, and isolation (National Health and Medical Research Council, 2010). The progress of human health care has seen good IC become an expectation of the general community with improving hand hygiene a sign of best practice (Grayson, Ryan, Havers, & Olsen, 2017).

In contrast, basic IC has not been applied systematically by the veterinary profession (J. Stull, 2016; J. W. Stull & Weese, 2015; Weese, 2011). An established culture of casual indifference toward basic hygiene practices has been well documented within veterinary practices (Attard et al., 2012; Morley, 2013) despite facing similar challenges as human health care facilities(Alder & Easton, 2005). Within small animal veterinary practices, there is a lack of regular IC plans and dedicated IC staff to monitor and implement protocols.

Infection control is needed in veterinary practice as poor IC poses a risk to animals as well as humans. Nosocomial outbreaks due to methicillin resistant Staphylococcus pseudintermedius (Grönthal et al., 2014), and feline calicivirus (Australian Veterinary Association, 2016; Reynolds et al., 2009) are well recognised. Pathogens such as Salmonella spp. have been linked with nosocomial outbreaks (Walther,

This article is protected by copyright. All rights reserved Tedin, & Lübke-Becker, 2017) as well as presenting a zoonotic risk to both staff and clients (J. W. Stull & Weese, 2015; H. Wright et al., 2005).

Antimicrobial resistance (AMR) has been irrefutably linked with infection control. Hand hygiene can help with reducing nosocomial infections and thus reduce the need for antimicrobial use, which reduces the emergence and spread of AMR (World Health Organization, 2015). AMR is a global issue that requires a coordinated effort between human and veterinary practitioners as it impacts on both human and animal health (Prescott, 2008). The World Health Organisation has highlighted the need for interventions in the veterinary sector to support a global strategy (World Health Organization, 2015, 2016).

Objectives The aim of this systematic review was to determine personal and environmental IC practices used in small animal veterinary workplaces worldwide. The two objectives were: to determine the range of approaches to IC practices, and secondly, to identify the efficacy of IC interventions to improve IC practices.

Methods

Protocols The Preferred Reporting Items for Systematic reviews and meta-Analyses (PRISMA) Statement for reporting Systematic Reviews checklist (Liberati, Altman, Tetzlaff, & Mulrow, 2009) was utilised to structure this systematic review. The STROBE-Vet statement checklist was used to comprehensively assess the studies for quality (Sargeant et al., 2016).

Information sources Details of the search terms and electronic databases used for this review are provided in Table 1. Each database has different search functions so alternate search terms were required to capture a workable number of studies. Boolean operators were utilised in all searches. Data searches commenced in February 2016 and concluded in December 2016. A follow up search performed in August 2018 identified no additional studies for inclusion. Additional studies were identified by hand searching the bibliography of included studies. Endnote X7.4 (1988-2015 Thomson Reuters) was used to store all studies and documents retrieved.

The population of interest included veterinarians and veterinary staff from generalist and specialist small animal practices. Peer reviewed primary research studies that examined clinical practice or management of IC practices were included.

This article is protected by copyright. All rights reserved Eligibility criteria Studies were eligible for inclusion if they involved behavioural IC practices of staff employed in veterinary clinics identified through reading of titles, abstracts and text scanning. These IC practices included hand hygiene, environmental cleaning, personal vaccination and the use of personal protective equipment. Two investigators (AW, SR) independently screened the title and abstract from the searches. Any disagreements were settled by discussion. Small animal responses had to be greater than 50% overall to be included in this systematic review. A summary of inclusion and exclusion criteria are listed in Table 2.

Study selection Data collection process and data items For each study that met the selection criteria for inclusion the following data were extracted: first author and year of publication, type of study, IC practice examined, if an intervention was included, numbers of participants, response rate and outcome. Attempts were made to obtain copies of questionnaires and intervention materials from the corresponding authors of the included studies.

Risk of bias Risk of bias was assessed using “The STROBE-Vet statement checklist”(Sargeant et al., 2016). The “Strengthening the Reporting of Observational Studies in Epidemiology-Vet (STROBE-Vet)” assessment tool assists in evaluating observational studies in “veterinary medicine related to health, production, welfare, and food safety” (Liberati et al., 2009).

Results

Study selection The study selection process is shown in Figure 1. A total of 1509 studies were identified from database searches, and a further 59 studies through the hand searching process, giving a total of 1615. Of these, 1251 were excluded after screening the title and abstract. A further 279 studies were excluded because they were policy documents or systematic reviews. The remaining 85 studies were critically assessed and a further 55 were excluded as they were descriptive or not a primary research study leaving 30 studies suitable for inclusion in the systematic review. The full text of the remaining 30 studies was read and a further 16 studies were excluded as they did not include behaviour change strategies. This left a total of 14 studies for inclusion in this review.

All studies reviewed were published from 2008 to 2016. No studies were found in the first 12 years of the search. Three studies (Dowd, Taylor, Toribio, Hooker, & Dhand, 2013; Lipton, Hopkins, Koehler, &

This article is protected by copyright. All rights reserved DiGiacomo, 2008; J. G. Wright, Jung, Holman, Marano, & McQuiston, 2008) included a combination of small animal (range 58% to 91%), large animal and equine veterinarians. One paper (Benedict, Morley, & Van Metre, 2008), interviewed individuals identifying as IC experts within their veterinary teaching hospital which included small and large animal facilities. Seven corresponding authors were contacted to obtain copies of their questionnaires with four providing copies and three authors not responding. One questionnaire was available as an appendix (Sparksman, Knowles, Werrett, & Holt, 2015).

Six studies were conducted in the USA, five studies in Canada, and two studies completed in Australia. One study was conducted in the United Kingdom.

The STROBE-Vet statement is designed for observational studies, of which there were five studies (M. E. Anderson, Sargeant, & Weese, 2014; M. E. Anderson & Weese, 2015; Shea & Shaw, 2012; Smith, Packman, & Hofmeister, 2013; Sparksman et al., 2015). The remaining nine studies were also assessed according to the statement to ensure continuity. Table 3 shows a summary of studies against each statement item. Each statement that was classified as completely attained was coded in white. If statements did not satisfy all or partly satisfied checklist items, they were categorised as partly attained and coded in grey. Any checklist items not attained were coded in black. Some items were classified as not applicable.

Research methods Descriptive studies (n=11) were the most common (79%) research designs, that employed questionnaires/surveys (electronic, paper, or telephone-based) (M. E. Anderson & Weese, 2016; Benedict et al., 2008; Dowd et al., 2013; Lipton et al., 2008; Murphy, Reid-Smith, Weese, & McEwen, 2010; Nakamura, Tompkins, Braasch, Martinez, & Bianco, 2012; Sellens et al., 2016; Smith et al., 2013; Sparksman et al., 2015; Weese & Faires, 2009; J. G. Wright et al., 2008). Video observation was used in two included papers in two separate studies, with one study investigating two areas of IC (environmental control and sharps management). The other study assessed the impact of a poster intervention (M. E. Anderson et al., 2014; M. E. Anderson & Weese, 2015). Direct observation in the workplace was used in two studies (Shea & Shaw, 2012; Smith et al., 2013).

It is not possible to combine outcome data from the included studies describing interventions to calculate a pooled estimate of efficacy because they each used a different methodology and outcome measure. The results of the two intervention studies (M. E. Anderson et al., 2014; Shea & Shaw, 2012) showed a significant improvement in hand hygiene compliance as a result of multimodal interventions (see Appendix 1). The outcomes of the third included intervention study (Smith et al., 2013) showed a small (2%) improvement in hand hygiene practices that was not statistically significant.

This article is protected by copyright. All rights reserved Hand hygiene was coded and assessed in multiple ways across four of the 14 studies. One of the 14 studies (J. G. Wright et al., 2008), developed their own unique arbitrary system to allocate a score to each respondent. The score was calculated according to their responses and linked to their IC practice. Two of the three intervention studies used modified versions of the World Health Organization hand hygiene tool (M. E. Anderson et al., 2014; Smith et al., 2013). The other included intervention study used a standardised coding system that was described (Shea & Shaw, 2012). The remaining included studies had no quantitative evaluation system.

Risk of bias The STROBE (Strengthening the Reporting of Observational Studies in Epidemiology)-Vet (Sargeant et al., 2016) statement is a 22 item tool that allows a systematic way to report on veterinary observational studies. A tool was not able to be found which addressed the diversity of studies in this review. The generalisability of STROBE-vet enabled it to be applied to these studies. While not animal populations, the items ensured comprehensive reporting in the veterinary setting. Each study was assessed individually according to each item, summarised in Table 3. Only one article successfully reported on all items (M. E. Anderson & Weese, 2015) . Items reported well by studies were; providing a background and rationale (item two), stating objectives (item three), presenting key elements of the study design (item four), describing study size (item ten), reporting outcomes for the study (item 15), providing estimates and parameters (item 16), summarising key results with reference to study objectives (item 18), interpreting results (item 20), and discussing the generalisability of the results (item 21).

Some items were less rigorously completed by the studies. Items not as thorough included the describing of study participants (item 14) which was partially attained by 11 studies (79%), with ten (71 %) studies providing reduced information regarding funding transparency (item 22). The funding source was not provided by two studies, a conflict of interest statement was lacking in eight studies and ethics approval was not discussed by three studies. Data sources and measurement (item eight) and description of statistical methods (item 12) were both partially attained by eight (57 %) studies. Item 22, funding transparency, was also poorly addressed with 10/14 (71%) not providing information for each of the five required sub-items. It was found that the studies did not report sufficiently on questionnaire development, validation and administration, data sources and measurement (item eight), with 8/14 (57%) partly addressing these criteria. Discussing statistical methods completely (item 12), particularly addressing missing data was omitted 8/14 (57%) times overall.

This article is protected by copyright. All rights reserved A total of one (1%) from 308 risk items were not attained. The risk item not attained was from one study (Sparksman et al., 2015). The author did not describe potential sources of bias in the study (item nine).

Study outcomes Study outcomes for hand hygiene, environmental control, sharps management, vaccinations for zoonotic infections and personal protective equipment are summarised in Table 4. Specific details of the outcomes of each included study are provided in Appendix 2.

Hand hygiene Hand hygiene was the most commonly included IC area and was the focus of nine out of 14 studies, with three studies describing interventions for hand hygiene. Three studies reported that hand hygiene was performed 42%-67% regularly between handling patients (Lipton et al., 2008; Nakamura et al., 2012; J. G. Wright et al., 2008), yet 86% of respondents thought it should be performed more frequently (Nakamura et al., 2012). A video observation study found that overall hand hygiene compliance was low at 14% (M. E. Anderson et al., 2014). Washing hands consistently before eating or drinking was observed to occur just over half of the time (55%) (J. G. Wright et al., 2008). The lowest hand hygiene compliance occurred before clean procedures such as needle administration or before patient care (M. E. Anderson et al., 2014; Smith et al., 2013). The greatest compliance occurred after “dirty” procedures and when tasks were performed in clinic procedural areas (M. E. Anderson et al., 2014; Smith et al., 2013). Veterinary support staff were found to have the lowest compliance in all staffing groups (M. E. Anderson et al., 2014) One included study found that 94% of staff agreed that hand hygiene was effective in reducing zoonotic risk (Dowd et al., 2013).

Soap and water was used frequently in hand hygiene (M. E. Anderson et al., 2014; Nakamura et al., 2012). Two studies investigated the use of alcohol based hand rub (ABHR) (Shea & Shaw, 2012; Sparksman et al., 2015). One study found a small increase in hand hygiene compliance after an educational campaign but noted a corresponding reduction in the use of gloves (Shea & Shaw, 2012; Smith et al., 2013). The other study found that surfaces were touched 29% of the time while gloves were worn with hand hygiene performed post removal only in 39% of cases (M. E. Anderson et al., 2014).

The most common deterrents to hand hygiene were high workload (Nakamura et al., 2012; Smith et al., 2013) or forgetting (M. E. Anderson & Weese, 2016). Other factors contributing to poor hand hygiene compliance included being of male gender (M. E. Anderson et al., 2014; M. E. Anderson & Weese, 2016) or not having an opportunity to perform hand hygiene (Smith et al., 2013). Wearing of rings and hand jewellery was a common behaviour and observed in 50% of veterinary technicians

This article is protected by copyright. All rights reserved (Nakamura et al., 2012). The wearing of rings and hand jewellery to work also increased the presence of microbial contamination (M. E. Anderson et al., 2014; Nakamura et al., 2012).

Environmental control Six studies focused on environmental control, including cleaning and disinfection, as well as IC guidelines and policy. One study (M. E. Anderson & Weese, 2015) found that practices reported disinfection of examination and surgical tables between patients 88% of the time. Further, contact time of disinfectants was less than or equivalent to 15 seconds.

Three studies found 53% to 70% of staff regularly consumed food and drink in animal handling areas (M. E. Anderson & Weese, 2015; Lipton et al., 2008; J. G. Wright et al., 2008). Two studies reported that only 14% of staff never had food and drink around animals (Lipton et al., 2008; J. G. Wright et al., 2008). The incidence of eating and drinking in the workplace reduced as the clinical experience of veterinarians increased (Lipton et al., 2008) .

The availability of dedicated isolation areas for infectious patients was investigated by three studies. They showed that isolation units were present in just over a third of the practices in Canada (Murphy et al., 2010), and just over half of the practices (companion, farm, equine) in Australia (Dowd et al., 2013). Nearly all (94%) veterinary teaching hospitals covered in the studies had isolation units (Benedict et al., 2008).

The availability of IC guidelines and/or policies was investigated in six included studies (M. E. Anderson & Weese, 2016; Benedict et al., 2008; Dowd et al., 2013; Lipton et al., 2008; Murphy et al., 2010; J. G. Wright et al., 2008). IC guidelines were not available in most of Canadian veterinary practices (16% to 31%) (M. E. Anderson & Weese, 2016; Lipton et al., 2008), and USA veterinary practices (79%) (J. G. Wright et al., 2008), while 89% of global veterinary teaching hospitals did have written IC policy documents (Benedict et al., 2008). Awareness of IC documents available in the workplace was poor with 49% of veterinary staff in Canada aware of their availability (M. E. Anderson & Weese, 2016). Formal IC programs were not available in veterinary practices in Canada (Murphy et al., 2010).

Education and training of veterinary staff was examined in one study. The Australian study found that veterinary nurses identified veterinarians and workplace protocols as the key sources for their IC information (Sellens et al., 2016).

Sharps management Sharps management was included in three studies (M. E. Anderson & Weese, 2015; Weese & Faires, 2009; J. G. Wright et al., 2008). All three included studies found a high incidence of needle stick

This article is protected by copyright. All rights reserved injuries (64% to 99%). Manual recapping of needles, unsafe disposal methods, lack of sharps disposal containers and injecting while restraining animals all contributed to injury (M. E. Anderson & Weese, 2015; Weese & Faires, 2009; J. G. Wright et al., 2008). Two included studies identified education is required to improve compliance for immediate, safe disposal (M. E. Anderson & Weese, 2015; Weese & Faires, 2009). One included study found only 20% of veterinary clinics had a written policy regarding needle stick injury. Staff had a perception that employers were indifferent to an injury occurring (Weese & Faires, 2009).

Vaccination for zoonotic infections Only two studies explored vaccination of veterinary staff to prevent zoonotic infections. One was a cross sectional survey of vaccination for Q Fever in Australia which found 74% of veterinarians and 29% of veterinary nurses were vaccinated. Barriers to vaccination included vaccine cost, lack of perceived risk, lack of time and finding a medical practitioner to administer the vaccine (Sellens et al., 2016). The other study from the USA reported up to 97% of veterinarians had received a rabies vaccination but less than 25% of veterinarians had undergone a rabies titre assay to assess immunity within the previous two years (J. G. Wright et al., 2008).

Personal protective equipment Four studies evaluated personal protective equipment (PPE). A study in Australia investigated 217 small animal veterinarians and found the use of PPE was inadequate in most scenarios except during post mortems (79%), surgery (80%) and dental procedures (84%) (Dowd et al., 2013). A study from Canada observed that 72% of veterinary staff complied with personal protective clothing (M. E. Anderson & Weese, 2015). Non-compliant clothing included the wearing of long sleeves or jumpers, open lab coats over street clothes and sleeves extending beyond the lab coat or scrub shirt (M. E. Anderson & Weese, 2015) . A study from the USA found that veterinarians were more likely to use PPE when animals were unwell or when handling high-risk products (J. G. Wright et al., 2008). Another study from the USA found 95% of veterinarians did not use respiratory or eye protection when examining obstetric patients (J. G. Wright et al., 2008) and veterinary staff from Canada had poor PPE implementation when examining animals exhibiting neurological signs in a rabies virus endemic area (Murphy et al., 2010).

Reported barriers to the use of PPE included cost, concerns regarding heat stress, lack of perceived risk, lack of availability (Dowd et al., 2013), as well as negative client perception (Dowd et al., 2013; J. G. Wright et al., 2008). Factors encouraging use of PPE were perceived risk, professional experience with zoonotic cases, concern regarding liability, recommendations by industry standards or guidelines, post graduate qualifications or working in government, research or laboratory

This article is protected by copyright. All rights reserved environments. There was a strong association with practices that did not have IC policies and subsequent low precaution awareness (Dowd et al., 2013).

Discussion

Summary of evidence This systematic review highlights the dearth of research conducted within the veterinary sector. Knowledge and practices associated with IC are lacking (Weese, 2011) despite an increased awareness of the benefits as a result of communication from veterinary associations (Australian Veterinary Association, 2017; Canadian Committee on Antibiotic Resistance, 2008). Human health care has far more resources than animal health care, such as dedicated staff, training and funding to support and promote adequate IC and prevention (Grayson et al., 2017; National Health and Medical Research Council, 2010), highlighting that more is needed in the veterinary sector. The review identified numerous areas within IC that can be improved.

Intervention studies The low number of intervention studies identified, and their limited scope (hand hygiene) highlights a major gap in the field of veterinary IC (Lund et al., 2016). Similar searches in human health care highlights many research studies. Suggestions for this inequity may be surmised from the different business and practice models. Human health care, within developed countries, tends to have staff dedicated to specific roles and budgets received from government entities (Kabene, Orchard, J, Soriano, & Leduc, 2006). Additionally, humans are at risk of infection with blood borne viruses, such as human immunodeficiency virus and hepatitis B virus. This potential exposure has necessitated a coordinated IC training and development program, albeit in a reactionary manner. Veterinary hospitals are generally owner-operated and smaller, despite providing a similar range of services to human health care providers, with costs and upkeep financed by the owner. The recent burgeoning of veterinary corporate practices may influence IC with policy and procedure development (Gyles, 2014). There are a number of zoonotic blood borne viruses in small animal practice that can be contracted from their patients, including Q Fever and Brucellosis (Australian Veterinary Association, 2017; Hensel, Negron, & Arenas-Gamboa, 2018; Sellens et al., 2016). While debilitating, they occur infrequently and are less likely to cause death, reinforcing the ingrained culture and poor IC adoption. Common zoonotic diseases, which include dermatophyte (fungal) infections, are easily managed (Australian infectious diseases advisory panel, 2016). Infection with more severe zoonotic pathogens is considered a low risk by many veterinary staff (Robin, Bettridge, & McMaster, 2017; Sellens et al., 2016). This perception influences the lack of personal protective equipment utilised or enforced by veterinary staff (Dowd et al., 2013).

This article is protected by copyright. All rights reserved There were substantial differences reported in hand hygiene compliance (14% -42%) in the three intervention studies (M. E. Anderson et al., 2014; Shea & Shaw, 2012; Smith et al., 2013). Factors responsible for this may be the differing methodologies employed by each researcher. Improved compliance may be partly attributed to the Hawthorne effect, where behaviour modification occurs due to awareness of participants being observed (James & Vo, 2010). The use of covert or video observation may reduce this effect and so provide more accurate findings over time. The hand hygiene training of each coder is not explicit. The type and frequency of training undertaken may affect the accuracy and consistency of monitoring compliance. Experience and confidence of the hand hygiene coders may also result in inconsistencies in recording of compliance rates.

The use of the WHO Hand Hygiene Guidelines provided a standardised format for use within the veterinary field (Verwilghen, 2018). Whether this tool is the most efficient for use in small animal veterinary practices has not been determined. Further studies are required to investigate if these guidelines can be adopted or require adaptation. No standard evaluation tool for hand hygiene or any other IC parameter is available within the veterinary field. Use of standardised criteria to code by is recommended to allow comparisons to be made between studies. In addition, the use of a tool such as the RE-AIM (reach, efficacy, adoption, implementation, maintenance) framework would be useful as it is highly applicable to research being conducted in practice (King, Glasgow, & Leeman-Castillo, 2010). Standardised criteria will allow for comparison between studies, veterinary practitioners and possibly other health care disciplines.

Multimodal interventions were the most successful in improving compliance (Shea & Shaw, 2012). However, the inclusion of behavioural change strategies was not discussed in any of the included studies. Sustaining long-term behaviour change must consider more than increasing knowledge alone (Abraham & Michie, 2008). Changing the attitudes and culture of a practice is recognised as a significant barrier to initiating change in many workplaces (M. E. Anderson & Weese, 2015; Cumbler et al., 2013). Implementing multimodal strategies within a behavioural change model will help to change individual practices and thus organisational culture (Cumbler et al., 2013; White, Jimmieson, et al., 2015). Research within human health care more frequently includes behaviour change models to achieve greater compliance for the long term (White, Jimmieson, et al., 2015; White, Starfelt, et al., 2015). None of the three intervention studies discussed any long-term follow up or maintenance of IC principles. The remaining 11 included studies displayed heterogeneity in IC practices assessed and the way in which they measured IC practices. This prevents any meaningful comparison and does not allow consensus or specific recommendations to be made.

This article is protected by copyright. All rights reserved Infection control practices The adoption of IC practices under the banner of standard precautions (hand hygiene, PPE, sharps management and environmental control) were consistently poor. In addition, the development of IC policies, guidelines and practices for hand hygiene were also poor and inconsistent for all geographic areas covered by the studies.

Effective hand hygiene is recognised as the most important IC intervention measure in both veterinary care and human health care. Hand hygiene is important as it is recognised as a significant factor contributing to microbial transfer (Australian Veterinary Association, 2017; Canadian Committee on Antibiotic Resistance, 2008; Grayson et al., 2017). The WHO has been instrumental in providing clear hand hygiene guidelines, information and teaching resources for human health care (World Health Organization, 2009). This review highlighted that poor practices such as the use of solid soap, lack of ABHR (Kingston, Slevin, O'Connell, & Dunne, 2017) and poor use of gloves is common amongst veterinary staff and that there is considerable scope for improvement (Australian Veterinary Association, 2017; Canadian Committee on Antibiotic Resistance, 2008).

Environmental control was only investigated by five studies and there was variation regarding the IC practices examined. Environmental control is important as it assists with reducing the risk of nosocomial and zoonotic infections, and the development of multi-resistant organisms. Practices such as inadequate disinfectant contact time and sharing of multi-use products between patients increase the risk for pathogenic transmission. The threat of multiresistant organism breakouts can be reduced with an effective environmental cleaning program (Walther et al., 2017).

Personal protective equipment provides an additional layer of defence in protecting the individual and the patient. Barriers precluding the use of PPE as part of daily practice include cultural attitudes, time and cost (M. E. C. Anderson, 2015). While the risk of blood borne disease transmission is low for veterinary staff, it remains a risk. The threat of emerging diseases from small animals may pose an additional risk (Chomel, 2014).

Vaccination requirements vary depending on country and work requirements. Individual attitudes were a key barrier to seeking vaccination and acknowledging susceptibility. Veterinary staff need to be better informed about required vaccinations to reduce risk. The lack of a single governing body to facilitate contact of all veterinary staff Australia wide was a key limitation identified (Sellens et al., 2016). More work is needed in this area to identify why staff are not undergoing vaccination and protecting themselves from contracting preventable zoonotic diseases.

This article is protected by copyright. All rights reserved Strengths and Limitations A strength of this review is that it critically examines IC practices in small animal veterinary practice. As health care practitioners, veterinary staff have the opportunity to refer to human health care which has a plethora of research articles to use as a baseline in the absence of similar veterinary studies.

Limitations relate to the few studies available. While some comparisons can be made with the human health care setting, caution must be exercised because of the many differences within the veterinary context. It is difficult to draw conclusions and provide recommendations from the small number of interventional studies. This review only examined small animal practice as equine and livestock practice differs substantially with regard to location of care, exposure risk, treatment procedures and infection control management.

Finding a tool to appraise each study individually proved challenging due to the range of study designs. There was no tool that was able to accommodate the range of heterogeneity present in the included studies. The STROBE-Vet, while modified for animal populations, had sufficient flexibility to allow analysis in a more generalised setting.

Recommendations Further research is required in the field of IC and prevention in order to reduce the risk of nosocomial infections and zoonotic diseases transmission. This research must be evidence based and replicable, regardless of the study design employed. Evidence-based studies will help with improving the quality of care as well as assessing the strength of the evidence. Observational studies, when conducted covertly, allow a true representation of behaviours occurring and may provide greater understanding of the underlying problem/s (Guest, 2014).

Due to the small number of studies, global cooperation will help to develop relationships and encourage the exchange of information and ideas. This will increase the available data which will aid in developing cohesive IC guidelines. These can be used for assessing the effectiveness of interventions. There is also a need for further systematic reviews investigating a broader cross-section of veterinary practices, such as large animal practice, required to identify all associated research conducted to date.

Veterinary associations and teaching institutions of both veterinarians and veterinary nurses / technicians need to place greater emphasis on the importance of IC, possibly through professional development and curriculum (Gould & Chamberlain, 1997). One suggestion would be to establish a

This article is protected by copyright. All rights reserved person and / or unit, supported by senior staff and management, to facilitate IC and provide support to practices. This will assist with implementing and reinforcing desirable practices.

As antimicrobial resistance becomes more of a concern in both veterinary and human health care, this too must be acknowledged. There is a need to explore the awareness of veterinary practitioners and the potential impact of antimicrobial prescribing and the management of patients with antimicrobial resistant infections (Browning, 2017; Hardefeldt et al., 2017; Zhuo et al., 2018).

A more consistent reporting structure for notifiable zoonotic diseases is needed so that parallels can be drawn within and between countries. This is unlikely to capture all cases of notifiable diseases as some members of the general public do not seek medical advice or manage and treat covertly. Evasive behaviours may occur as management of some diseases, such as brucellosis, which can recommend humane euthanasia in favour of treatment due to its potential zoonotic risk (D. James et al., 2017).

Conclusions The results of this systematic review highlight the lack of evidence necessary for the development of feasible IC guidelines and protocols for small animal veterinary practice. Further research is required to better characterise the barriers and opportunities to improving IC practices. In addition, well designed behavioural intervention studies are needed to inform the development of useable protocols and training materials for use in practice and veterinary schools

Conflict of interest statement

The authors declare that they have no affiliations with or involvement in any organisation or entity with any financial or non-financial interest in the subject matter or materials discussed in this manuscript.

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Appendix 1: Summary of studies used in Systematic review for infection control practices in companion animal veterinary practices – Intervention studies (n=3).

Authors, year Study population Study design Intervention Data collection and Outcomes measured Outcome of publication Recruitment Modality – intensity, duration (including participants, practices) (ref) Demographics Infection control practice examined Attrition Country Anderson, Veterinarians & Observational study Poster intervention Clinic Participation Overall, HH‡ compliance 14% (1,473/10,894). Sargeant & staff in companion with poster Two different designs. Clinics approached 135/1100 Reach 12.3% Compliance before patient contact 3% Weese, 2014 animal clinics. intervention Poster A in every exam room. Poster B Agree to participate 52/135 (38.5%) (123/4,377). (Anderson et displayed near three HH stations. Coded/usable data 38/52 (73%) Compliance after patient contact 26% al., 2014) Convenience Hand hygiene (1,145/4,377). sample Video observation Individual appointments Canada Cameras in place 14-19 working days Appointments coded n = 2278 Female staff were 1.75 times more likely to Posters mounted between 9-13 working HH Opportunities n = 10,894 perform HH after patient contact than male days post camera installation. Individuals n = 449 staff. Coding performed by one person. 1139 appointments pre-& post-poster intervention analysed Used WHO†-5 moments for HH protocol. When ABHR available, contact time for HH Clear protocol for “clean” (such as  HH attempts observed (n =1,353) shorter for veterinarians compared to injections, venepuncture or applying a - Contact time 1s with product 38% (1,353-509 = 844 HH technicians and other staff. clean bandage over a skin lesion) & attempts) “dirty” (such as ear cleaning, contact with - Complete coding observed 45% (379/844) Soap & water is used most often, even when faeces or abscess drainage) veterinary * Total HH compliance (total number of opportunities for which a HH ABHR is available. procedure in HH monitoring study. attempt was observed divided by the total number of opportunities observed) 14% (1,473/10,894). Overall, HH compliance low & found to be the  HH prior to patient contact was 3% (123/4,377) & after “dirty” lowest before “clean” procedures. procedures was 26% (1,145/4,377). Posters did not have a significant effect on HH compliance. Surveys - follow up Distributed to staff (up to 20 per clinic) at each clinic. – 289/465 (62%) from 37/38 clinics

Attrition 3% (1 clinic)

HH posters put up in last week of study were noticed by 94% (272/289).

Shea & Shaw, Veterinary health Pre-Post study Multimodal 4-week educational Data Collection: A multimodal education campaign was 2012 (Shea & care providers design of campaign. HH observed covertly by 4 anonymous observers over two shifts successful in increasing total number of Shaw, 2012) (faculty, residents, multimodal observed, correct HH interactions from 21% to interns, students & educational Education, slogan, educational materials, Pre-educational campaign 42%. USA technicians) in campaign with 4- posters, reminder signs, presentation, Proper HH practices 21% (117/568 interactions) single small animal week post online training module & HH discussion ABHR used 6.0% (34/568 interactions) Staff using ABHR§ increased from 6.0% to university hospital completion of in new staff orientation. Glove use 6.0% (34/568 interactions) 36%. campaign follow up. Convenience Post educational campaign Glove use was low (6%) pre-intervention sample Hand hygiene Proper HH practices 42% (78/187 interactions) observations & reduced to less than 1% post- ABHR used 36% (67/187 interactions) intervention observations. Glove use 1% (1/187 interactions)

Campaign engagement Presentation attendance 42% Online training module completed 24%

† World Health Organization ‡ Hand Hygiene § Alcohol based hand rub

Appendix 2: Summary of studies used in Systematic review for infection control practices in companion animal veterinary practices – Descriptive studies (n = 11)

Authors, year of Study Study design Response rate Observation data publication (ref) population Outcomes Country Attrition

Anderson & Weese, Veterinarians / Observational Clinics approached 135/1,100 Sharps handling Sharps handling 2015 Veterinary study (3 wk) Response rate 12.3%. 36% (17/47) approved sharps container readily available Disposal visible sharps prior to end of technicians - Coded / usable data 47/51 in exam room appointment significantly associated with Canada primary care All data coded by 26% (12/47) sharps disposal container in cupboard or availability of approved container. companion one investigator Attrition 8% drawer Environmental cleaning animal veterinary 30% (14/47) no apparent sharps disposal container in Table cleaning significantly associated with clinics. Observed 2713 appointments exam room. Sharps taken elsewhere or placed in open patient contact with exam table & floor Infection control Total of 535 individuals with tray/cup for disposal. cleaning with patient contact with exam practices 4,903 staff animal contacts. 0.4% (4/1137) – recapping with “scoop” technique room floor. Convenience Sharps handling 26% (350/1,353) - uncapping needle using mouth PPC‡ sample Environmental 84% (1,137/1,353) – recapping needle Appropriate PPC significantly associated cleaning 17% (237/1,359) bare sharp being left out with being a veterinarian or technician PPE† 1 needle stick injury observed compared to other staff, but not with Environmental cleaning gender. No significant difference between Exam table cleaned & exam room floor mopped beginning veterinarians & technicians. & end of day, description of frequency unclear. Overall 7% (178/2,646) exam table cleaned > once Despite low numbers of approved & Animal contact - exam table 24% (659/2,713), exam room available sharps containers in clinics, floor 28% (748/2713) both 48% (1,295/2,713). frequent recapping of sharps & uncapping PPC needles by mouth, the overall needle stick 72% (3518/4,903) appropriate PPC worn for staff-animal incidence rate is very low. contacts. Cleaning of examination tables significantly 21 - 99% range of compliance for appropriate PPC per associated with patient contact. clinic. Use of appropriate PPC was role specific

† Personal protective equipment ‡ Personal protective clothing

and requires greater consistency in general.

Anderson & Weese, Veterinary Clinic Questionnaire Clinics approached 135/1100 356/578 (62%) participants (Potentially constrained by maximum HH considered very important. Human hospitals being 2016 staff – primary Response rate 12.3%. participation rate) the most important & veterinary clinics & community care companion Written. Agree to participate 51/135 Observations being similar. Canada & mixed Maximum of 20 clinics (37.8%) Importance of HH§ (scale of 1 not important to 7 very Most common reasons for not performing HH: respondents per Coded / usable data 49/51 important) forgetting, skin damage or being too busy, a small Convenience clinic. clinics Attrition 4% 87% (308/355) – hand hygiene in veterinary clinics very number using gloves in place of performing HH. sample. Distribution & important collection at 95% (336/355) – hand hygiene in human hospitals very Greater education required to improve HH in the discretion of important workplace. clinic staff when 86% (306/355) – hand hygiene in the community very HH considered important yet not practiced >20. important consistently.

Hand hygiene Reasons for not performing hand hygiene Clinic Practices 40% (141/353) – forgetting to do so 22% (78/353) – skin damage 21% (78/353) – being too busy 5% (17/353) - inconvenient HH stations Clinic practices 49% (163/335) of respondents were aware of written clinic infection control manual or policies.

Benedict, Morley & International Telephone Eligible institution (n = 39) Observations Most AVMA accredited institutions have IC policies & Van Metre, 2008 study of interviews (North America (30/31), EU (n 84% (32/38) of institutions had IC†† program overseen by designated IC officers. veterinary = 4/4), Australia (n = 3/3), New an IC committee. Despite IC measures in place, there were still high biosecurity Infection control Zealand (n =1/1) 89% (34/38) had written policy documents. levels of nosocomial outbreaks & zoonotic disease experts practices Usable data 38/39 (97%) 84% (32/38) had a single person responsible for leading exposure. Biosecurity Institution Attrition 3% IC activities. IC training was not conducted in more than half of the Convenience Nosocomial Total interviewed - 50/52 89% (32/36) had documents for cleaning & disinfecting AVMA accredited institutions.

§ Hand hygiene †† Infection control

sample infections individuals the hospital environment. Eligible study Zoonotic Participant attrition 4% 42% (16/38) required staff to complete IC training population – diseases 92% (33/36) had policies for PPE use schools & 82% (31/38) reported nosocomial infection outbreaks in colleges of the preceding five years & 45% (17/38) > 1 outbreak. veterinary 50% (19/38) reported significant health problems medicine attributed to zoonotic disease in preceding two years. accredited by 94% (34/36) had small animal isolation facilities. AVMA** that 86% (43/50) believe differences in hygiene standards operated a among AVMA accredited institutions veterinary teaching hospital

Dowd, Taylor, Veterinarians Questionnaire Response rate 42.4% Observations Use of PPE inconsistent in high-risk situations. Toribio, Hooker & (344/812) Use of adequate PPE Cultural issues such as workplace policies & practices Dhand, 2013 Convenience Infection control 63.2% (203/321) worked in 79.5% (252/317) - surgery (overalls/gown & gloves) as well as individual perceptions influence PPE use. sample practices small animal / companion 79.1% (253/320) – post mortems (overalls/gown & gloves) Australia 2011 Australian PPE animal 50.3% (145/288) – conception & parturition procedures Veterinary (overalls/gown & gloves) Association 24.2% (80/331) – handling animal faeces & urine Conference, (overalls/gown & gloves) English speaking 84% (257/306) – dental procedures (overalls/gown & gloves & face shield / goggles) IC practices of veterinarians 25.3% - undergone staff training for use of PPE 10.7% - deterrent to use of PPE is cost of PPE kits 11.8% - deterrent to use of PPE is the negative client perception about the vet wearing PPE 52.8% - practice stringent IC practices only if they are believed to be necessary 24.3% - believe their colleagues are being over cautions

** American Veterinary Medical Association

when they use PPE

Lipton, Hopkins, Veterinarians Questionnaire Response rate 83% (376/454) Observations IC practices such as hand washing & environmental Koehler & Coded / usable data 98% 67% (246/366) - Always wash hands between handling cleaning require improvement through education & DiGiacomo,2008 Convenience Infection control (370/376) Attrition 1.6% individual animals enhanced awareness. sample practices (6/376) 88% (310/352) - Examination & treatment tables always USA All clinical Small animal practitioners disinfected between patients medicine licensed 91% (336/370) 53% (193/346) - Eating & drinking in animal handling in King County, areas daily Washington. 14% (50/364) - Never eat or drink in animal handling areas 31% (112/360) - No written IC guidelines in the practice Murphy, Reid- Veterinarians & Questionnaire Clinics approached 16% Observations IC programs and staff are required in veterinary Smith, Weese & veterinary (121/766) Attrition rate17% 0% (0/101) - IC program or individual involved with IC practices. McEwen, 2010 technicians Infection control (20/121) 65% (66/101) - No designated isolation area Dedicated isolation areas will help with preventing the practices Practice Response rate 13.2% 61% (40/66) - No specific IC measures when hospitalising spread of infectious diseases. Canada Companion Environmental (101/766) possible or known infectious case Additional training of veterinary staff is required in IC animal veterinary cleaning & Companion animal 89% 26% (26/101) - attempt to physically separate infectious practices. practices disinfection (90/101) patient from remaining hospital patients southern Ontario 9% (9/101) - Only IC measure is to physically separate infectious patient from remaining hospital patients Convenience 8% (8/101) - use of disposable gloves or booties when sample handling known or suspected infectious patient.

Nakamura, Veterinary Questionnaire Coded / usable data - 182 Observations HH practices amongst veterinary technicians were Tompkins, Braasch, technicians & respondents (number HH practices poor. Martinez & Bianco, veterinary support Hand Hygiene distributed unknown) 42% (76/182) regularly washed their hands every time Most common reason for not performing HH was 2012 staff (veterinary Attrition: Unable to calculate between handling patients. being too busy. assistants, kennel 85% (154/182) believe they should wash their hands more The HH rates of veterinary technicians & support staff USA staff) frequently were found to be comparable to those of veterinarians 4 small animal 19% (35/182) reported shortage of HH agents availability and staff in human hospitals. speciality 85% (154/182) reported hand soap is the most commonly There was an expectation that veterinarians teach hospitals & 14 used HH agent veterinary technicians & support staff about the small animal Reasons for not washing hands more frequently importance of HH.

general practice 73% (132/182) – being too busy hospitals HH education Selection process 53% (96/182) reported veterinarians educated them about of practices not importance of good HH practices identified. 80% (37/46) reported being educated about importance of HH in school Convenience sample

Sellens, Norris, Veterinarians & Questionnaire Coded/usable data 58% veterinarians small animal practice. Veterinarians & veterinary nurses near 100% Dhand, Heller, veterinary nurses 1742/16,000 (Estimated 7400 75% veterinary nurses small animal practice. agreeance on value of vaccination & Q fever being Hayes, Gidding & All veterinarians Q Fever employed veterinarians & Observations serious disease. Willaby, 2016 & veterinary vaccination 8600 veterinary nurses). Attitudes towards vaccination Perception not carried through to action with only 27% nurses in (Veterinary nurses in Western 97% veterinarians & veterinary nurses agreed vaccines seeking vaccination. Australia Australia >18 yrs. Australia are registered with are important in prevention of disease. Veterinary nurses reported lower levels of awareness of age & currently the Western Australia state Knowledge & perceptions of Q fever vaccination & disease & knowledge. or recently veterinary board. Veterinary 98% of veterinarians & veterinary nurses agreed Q fever employed in a nurses in other states & is serious disease with significant health consequences. veterinary territories in Australia are not Exposure to Coxiella burnetti workplace. registered in a central registry) 11% (93/850) of veterinarians & 25% (201/793) of All states & Response rate 10.1% (890 veterinary nurses did not know level of exposure. territories veterinarians & 852 veterinary Vaccination status & barriers to vaccination represented. nurses) 74% (587/796) of veterinarians were either vaccinated or had sought Q fever vaccination Convenience Increased to 78% (562/721) of Australian veterinary sample school graduates receiving vaccination. 29% (199/688) of veterinary nurses were either vaccinated or had sought Q Fever vaccination. 81% of veterinarians received Q fever vaccination as part of university course requirements. 43% of veterinary nurses received the Q fever vaccination as part of job requirements. 7% (57/796) veterinarians & 30% (205/688) veterinary nurses not aware that Q fever vaccine existed.

Sparksman, Veterinary nurses Questionnaire. Coded / usable data 19.5% HH ABHR was the most commonly used HH agent Knowles, Werrett & (78/400) 68%( 50/74) stated ABHR‡‡ was the most common hand Holt, 2015 Convenience Hand hygiene Attrition 1% (4/400) antiseptic agent sample and United Kingdom random sample

Weese & Faires, Veterinary Questionnaire Coded / usable data 15% Observations NSIs are very common with 4% requiring medical care 2009 (Weese & technicians (226/1500) 93% (210/226) veterinary technicians have had at least 1 & 1% having time off work. Faires, 2009) Members of Needle stick NSI Most NSIs are not reported to employers. Ontario injuries 59% (133/226) exposed to animal blood one or more High-risk behaviours such as recapping needles are Canada Association of times due to NSI frequently performed. Veterinary 79% (178/223) always or usually recapped a needle Technicians manually 12% (23/226) did not have immediate access to a sharps container in area where needles used Convenience 4.0% (9/226) always placed needles in a temporary sample storage container prior to proper disposal 20% (45/226) stated place of employment had written policy regarding NSIs 24% (55/226) had a policy mandating reporting of NSIs Reasons for not reporting NSI to employer 36% (82/226) not thinking about it 28% (64/226) employer not expressing a need to know 24% (54/226) thinking reporting would not have any effect 9% (20/226) considering injury insignificant 10% (23/226) always reported NSIs 0% Reported number of safe injection devices (retractable needles, hinged caps) in use Wright, Jung, Veterinarians Questionnaire Coded/ usable data Eligible veterinarians 70% (48,548/69,029 AVMA members) (48,548 The use of PPE is poorly adopted & high-risk Holman, Marano & Responses 2133/5168 (41%) clinicians) behaviours such as handling bodily fluids are McQuiston 2008 Random selection Infection control Response attrition 59% Further broken down into 3 groups: commonly practiced by veterinarians.

‡‡ Alcohol based hand rub

of eligible AVMA practices – (3035/5168) 2,414/29,553 (8%) small animal veterinarians HH is reported to be practiced frequently before USA veterinarians PPE 1,287/2,045 (64%) large animal veterinarians activities such as eating & drinking despite a large Hand hygiene 1,467/2,404 (61%) equine veterinarians (n = 5168) number having food in clinical areas. Sharps Final sample population of 1842 veterinarians comprising: The adoption of written IC policies & training was management 1070/29,553 (3.6 %) small animal suggested to improve compliance. Rabies 316/2,045 (15.5%) large animal vaccination 456/2,404 (19%) equine

Observations A variety of IC practices were examined in this survey. Only small animal responses were included for this review 31% (247/797) - Written infection control policy at the practice 93.1% (995/1,069) - Washed hands before eating, drinking or smoking at work (mostly or always) 13.8% (147/107) Never eating or drinking in animal handling areas 48.4% (516/1,066) Washing / sanitising hands between patient contacts(always) 32.0%15 (341/1,066) Always recapping needles pre- disposal 95.6% (1022/1,069) Always disposing of needles in approved sharps container 6.9% (73/1,066) Handling of faecal samples (no special precautions) 17.2% (183/1,064) Handling of urine samples (no special precautions) 6.5% (60/929) Handling products of conception or assisting with parturition (no special precautions)

Table 1. Search strategies and databases used in systematic review of infection control practices in small animal veterinary practices

Database Search strategies and search terms Embase “Systematic review” AND veterinary AND infection “Systematic review” AND veterinary OR veterinarian AND “infection control” AND zoonoses OR zoonotic OR zoonosis Google “Systematic review” and veterinary AND zoonosis or zoonoses or zoonotic

Google Scholar Veterinary or veterinarian and “infection control” "veterinary" AND "infection control" NOT large animal NOT "farm animal" NOT cow or cattle or bovine NOT horse or equine NOT sheep NOT poultry or chicken “Systematic review” AND veterinary AND “infection control” AND zoonoses NOT horses or equine IVIS (International “Systematic review” AND “infection control” AND zoonoses Veterinary Information Service) PubMed Using MeSH terms - Infection control, Subheading veterinary Nosocomial AND veterinary, NOT pig / swine / porcine / sheep / equine / horse / cow / cattle / bovine / poultry “Systematic review” AND veterinary AND infection control “Systematic review” AND “zoonoses or zoonosis or zoonotic” AND veterinary Veterinary OR veterinarian AND “infection control” in title or abstract NOT cattle, bovine, horses, equidae, equine, sheep or poultry Science Direct Veterinary or veterinarian and “infection control” in title or abstract Veterinary or veterinarian and “zoonoses or zoonosis” or nosocomial in title or abstract “Systematic review” in title AND veterinary infection control. Large animal excluded. “Systematic review” in title AND veterinary* OR zoonos* or nosocomial OR HAI or hospital acquired infection Scopus “systematic review” AND veterinary AND nosocomial OR zoonoses OR Infection control VetMed Resource Veterinary or veterinarian and “infection control” in abstract NOT cattle, cow, bovine, horses, equine, or poultry

Systematic review AND veterinary and infection control and zoonoses VIN (Veterinary Veterinary or veterinarian and “infection control” Information Network) NOT cattle, cow, bovine, horse, equine, poultry, chicken, sheep Web of Science Veterinary OR veterinarian AND “infection control” Limits – English language studies only No studies with large animals, farm animals, bovine, caprine, ovine, equine, fish or sea creatures.

Table 1. Inclusion and exclusion criteria for studies included in this systematic review of infection control practices in small animal veterinary practices

Inclusion criteria Exclusion criteria Small animals (dogs, cats, pocket pets, caged Farm animals, including cattle, sheep, goats, pigs, birds, and local wildlife) poultry Generalist and specialist small animal practices Equines English studies Non-English studies Published 1996 to 2016 Policy, government documents, Conference proceedings (unless peer reviewed) Peer reviewed studies Descriptive studies Infection control practices including behaviour or Studies not assessing clinical practice management of infection control practices Reviewing behaviour and/or behaviour change in a clinical setting Primary research study

Table 1 Bias summary for studies relating to infection control in veterinary practices using the Vet-STROBE checklist. (Key: No shading - all criteria attained, Grey – criteria partly attained, Black – criteria not attained, N/A – not applicable)

Items on STROBE-Vet Checklist (Sargeant et al., 2016)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Title abstract and Background/rationale Objectives design Study Setting Participants Variables sources Data Bias size Study Quantitative variables Statistical methods Participants confounders data & Descriptive onexposures potential Outcomedata Main results Other analyses results Key & limitationsStrengths Interpretation Generalizability Funding

transparency

/measurement

Article authors

Anderson, Sargeant & Weese, 2014

Anderson & Weese, 2015 N/A

Anderson & Weese, 2016 N/A

Benedict, Morley & Van Metre, 2008 N/A

Dowd, Taylor, Toribio, Hooker & Dhand,

2013

Lipton, Hopkins, Koehler & DiGiacomo, 2008 N/A

Murphy, Reid-Smith, Weese & McEwen, N/A 2010

Nakamura, Tompkins, Braasch, Martinez &

Bianco, 2012

Sellens, Norris, Dhand, Heller, Hayes, N/A Gidding, Willaby, Wood & Bosward, 2016

Shea & Shaw, 2012 N/A

Smith, Packman & Hofmeister, 2013 N/A

Sparksman, Knowles, Werrett & Holt, 2015 N/A

Weese & Faires, 2009 N/A

Wright, Jung, Holman, Marano &

McQuiston, 2008

Table 1. Summary of studies and methodology categorised by infection control practice. Hand hygiene Environmental Sharps Q Fever PPE Total control management Observation Shea & Shaw, 2012 2 Smith, Packman & Hofmeister, 2013 Video Anderson, Sargeant & Anderson & Anderson & Anderson & 4 observation Weese, 2014 Weese, 2015 Weese, 2015 Weese, 2015 Questionnaire Anderson & Weese, Benedict, Weese & Sellens, Dowd, Taylor, 19 (paper, on 2016 Morley & Van Faires, 2009 Norris, Toribio, Hooker line, phone) Dowd, Taylor, Toribio, Metre, 2008 Wright, Jung, Dhand, & Dhand, 2013 Hooker & Dhand, 2013 Dowd, Taylor, Holman, Hayes, Murphy, Reid- Lipton, Hopkins, Koehler Toribio, Hooker Marano & Gidding & Smith, Weese & & DiGiacomo, 2008 & Dhand, 2013 McQuiston, Willaby, McEwen, 2009 Nakamura, Tompkins, Lipton, Hopkins, 2008 2016 Wright, Jung, Braasch, Martinez & Koehler & Wright, Holman, Bianco, 2012 DiGiacomo, Jung, Marano & Smith, Packman & 2008 Holman, McQuiston, 2008 Hofmeister, 2013 Murphy, Reid- Marano & Sparksman, Knowles, Smith, Weese & McQuiston, Werrett & Holt, 2015 McEwen, 2009 2008 Wright, Jung, Holman, Wright, Jung, Marano & McQuiston, Holman, 2008 Marano & McQuiston, 2008 Intervention Anderson, Sargeant & 3 Weese, 2014 Shea & Shaw, 2012 Smith, Packman & Hofmeister, 2013 Total 13 6 3 2 4 28 Note: The total number of interventions (28) is greater than the total number of studies (14) as a number of studies included interventions in more than one area of infection control practice and used more than one criteria for evaluation.

Figure 1 Summary of study selection and exclusion (n = number)