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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Vet. Sci.</journal-id>
<journal-title>Frontiers in Veterinary Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Vet. Sci.</abbrev-journal-title>
<issn pub-type="epub">2297-1769</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fvets.2022.1087052</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Veterinary Science</subject>
<subj-group>
<subject>Systematic Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Hospital-acquired and zoonotic bacteria from a veterinary hospital and their associated antimicrobial-susceptibility profiles: A systematic review</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name><surname>Sebola</surname> <given-names>Dikeledi C.</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/2010555/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Oguttu</surname> <given-names>James W.</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/984401/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Kock</surname> <given-names>Marleen M.</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/425261/overview"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>Qekwana</surname> <given-names>Daniel N.</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="corresp" rid="c001"><sup>&#x0002A;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/595143/overview"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Section Veterinary Public Health, Department of Paraclinical Sciences, Faculty of Veterinary Science, University of Pretoria</institution>, <addr-line>Pretoria</addr-line>, <country>South Africa</country></aff>
<aff id="aff2"><sup>2</sup><institution>Department of Agriculture and Animal Health, College of Agriculture and Environmental Sciences, University of South Africa</institution>, <addr-line>Johannesburg</addr-line>, <country>South Africa</country></aff>
<aff id="aff3"><sup>3</sup><institution>Department of Medical Microbiology, University of Pretoria</institution>, <addr-line>Pretoria</addr-line>, <country>South Africa</country></aff>
<aff id="aff4"><sup>4</sup><institution>Tshwane Academic Division, National Health Laboratory Service</institution>, <addr-line>Pretoria</addr-line>, <country>South Africa</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Faham Khamesipour, Shahid Beheshti University of Medical Sciences, Iran</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: Babafela Awosile, Texas Tech University, United States; Manuela Oliveira, Universidade de Lisboa, Portugal</p></fn>
<corresp id="c001">&#x0002A;Correspondence: Daniel N. Qekwana &#x02709; <email>nenene.qekwana&#x00040;up.ac.za</email></corresp>
<fn fn-type="other" id="fn001"><p>This article was submitted to Veterinary Infectious Diseases, a section of the journal Frontiers in Veterinary Science</p></fn></author-notes>
<pub-date pub-type="epub">
<day>09</day>
<month>01</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2022</year>
</pub-date>
<volume>9</volume>
<elocation-id>1087052</elocation-id>
<history>
<date date-type="received">
<day>01</day>
<month>11</month>
<year>2022</year>
</date>
<date date-type="accepted">
<day>19</day>
<month>12</month>
<year>2022</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2023 Sebola, Oguttu, Kock and Qekwana.</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Sebola, Oguttu, Kock and Qekwana</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p></license> </permissions>
<abstract>
<sec>
<title>Background</title>
<p>Hospital-acquired infections (HAIs) are associated with increased mortality, morbidity, and an economic burden due to costs associated with extended hospital stays. Furthermore, most pathogens associated with HAIs in veterinary medicine are zoonotic. This study used published data to identify organisms associated with HAIs and zoonosis in veterinary medicine. Furthermore, the study also investigated the antimicrobial-susceptibility profile of these bacterial organisms.</p>
</sec>
<sec>
<title>Methods</title>
<p>A systematic literature review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. Search terms and five electronic databases were used to identify studies published over 20 years (2000&#x02013;2020). The risk of bias was assessed using the &#x0201C;Strengthening the Reporting of Observational Studies in Epidemiology-Vet&#x0201D; (STROBE-Vet) checklist.</p>
</sec>
<sec>
<title>Results</title>
<p>Out of the identified 628 papers, 27 met the inclusion criteria for this study. Most studies (63%, 17/27) included were either from small animal or companion animal clinics/hospitals, while 5% (4/27) were from large animal clinics/hospitals inclusive of bovine and equine hospitals. Hospital-acquired bacteria were reported from environmental surfaces (33%, 9/27), animal clinical cases (29.6%, 8/27), and fomites such as cell phones, clippers, stethoscopes, and computers (14.8%, 4/27). <italic>Staphylococcus</italic> spp. was the most (63%; 17/27) reported organism, followed by <italic>Escherichia coli</italic> (19%; 5/27), <italic>Enterococcus</italic> spp. (15%, 4/27), <italic>Salmonella</italic> spp. (15%; 4/27), <italic>Acinetobacter baumannii</italic> (15%, 4/27), <italic>Clostridioides difficile</italic> (4%, 1/27), and <italic>Pseudomonas aeruginosa</italic> (4%; 1/27). Multidrug-resistant (MDR) organisms were reported in 71% (12/17) of studies linked to Methicillin-resistant <italic>Staphylococcus aureus</italic> (MRSA), Methicillin-resistant <italic>Staphylococcus pseudintermedius</italic> (MRSP), <italic>Enterococcus</italic> spp., <italic>Salmonella</italic> Typhimurium<italic>, A. baumannii</italic>, and <italic>E. coli</italic>. The <italic>mec</italic>A gene was identified in both MRSA and MRSP, the <italic>bla</italic>CMY-2 gene in <italic>E. coli</italic> and <italic>Salmonella</italic> spp., and the <italic>van</italic>A gene in <italic>E. faecium</italic> isolate. Six studies reported organisms from animals with similar clonal lineage to those reported in human isolates.</p>
</sec>
<sec>
<title>Conclusion</title>
<p>Organisms associated with hospital-acquired infections and zoonosis have been reported from clinical cases, environmental surfaces, and items used during patient treatment and care. <italic>Staphylococcus</italic> species is the most reported organism in cases of HAIs and some isolates shared similar clonal lineage to those reported in humans. Some organisms associated with HAIs exhibit a high level of resistance and contain genes associated with antibiotic resistance.</p>
</sec></abstract>
<kwd-group>
<kwd>hospital acquired infections (HAIs)</kwd>
<kwd>zoonosis</kwd>
<kwd>veterinary</kwd>
<kwd>antimicrobial resistance (AMR)</kwd>
<kwd>nosocomial</kwd>
<kwd>antimicrobials</kwd>
<kwd>multi-drug resistance</kwd>
</kwd-group>
<counts>
<fig-count count="1"/>
<table-count count="6"/>
<equation-count count="0"/>
<ref-count count="73"/>
<page-count count="14"/>
<word-count count="8379"/>
</counts>
</article-meta>
</front>
<body>
<sec id="s1">
<title>1. Introduction</title>
<p>Hospital-acquired infections (HAIs) in both veterinary and human medicine are associated with increased mortality, and morbidity, and are an economic burden due to the increased cost of extended hospital stay and treatment options (<xref ref-type="bibr" rid="B1">1</xref>, <xref ref-type="bibr" rid="B2">2</xref>). The most reported HAIs include surgical wounds, urinary tract, and gastrointestinal infections (<xref ref-type="bibr" rid="B1">1</xref>&#x02013;<xref ref-type="bibr" rid="B3">3</xref>) and are often associated with bacteria such as <italic>Enterococcus</italic> species (spp.), <italic>Escherichia coli, Staphylococcus</italic> spp., <italic>Enterobacter</italic> spp., <italic>Klebsiella</italic> spp., <italic>Acinetobacter</italic> spp., and <italic>Pseudomonas</italic> spp. (<xref ref-type="bibr" rid="B3">3</xref>&#x02013;<xref ref-type="bibr" rid="B6">6</xref>).</p>
<p>Available evidence suggests that HAIs associated with <italic>Enterococcus</italic> spp., <italic>Escherichia coli, K. pneumoniae</italic>, and <italic>S. aureus</italic> are on the increase in veterinary medicine (<xref ref-type="bibr" rid="B7">7</xref>&#x02013;<xref ref-type="bibr" rid="B10">10</xref>). There are also reports of vancomycin-resistant enterococci (VRE), multidrug-resistant (MDR) <italic>E. coli</italic>, carbapenem-resistant <italic>A. baumannii</italic>, carbapenem-resistant <italic>P. aeruginosa</italic>, carbapenem-resistant and extended-spectrum &#x003B2;-lactamase (ESBL) producing <italic>Enterobacteriaceae</italic> (<xref ref-type="bibr" rid="B3">3</xref>&#x02013;<xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B11">11</xref>&#x02013;<xref ref-type="bibr" rid="B13">13</xref>), with limited treatment options and poor prognosis (<xref ref-type="bibr" rid="B1">1</xref>, <xref ref-type="bibr" rid="B5">5</xref>, <xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B11">11</xref>, <xref ref-type="bibr" rid="B13">13</xref>). It is estimated that 60% of emerging infectious diseases are likely to come from animals (<xref ref-type="bibr" rid="B14">14</xref>, <xref ref-type="bibr" rid="B15">15</xref>). Of concern is that bacteria associated with HAIs in veterinary settings could be contributing to the emergence of these new diseases (<xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B16">16</xref>). Since the veterinary hospital environment is a human-animal interface, it remains a potential source of zoonotic pathogens (<xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B17">17</xref>). Therefore, veterinary healthcare workers and animal owners are at an increased risk of contracting various zoonotic infections (<xref ref-type="bibr" rid="B14">14</xref>, <xref ref-type="bibr" rid="B15">15</xref>). This is likely to put financial stress on the human health system especially in developing countries (<xref ref-type="bibr" rid="B18">18</xref>). In view of this, continuous surveillance of hospital-acquired and zoonotic pathogens in veterinary medicine should be done to better quantify the risk of transmission to personnel and animal owners (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>).</p>
<p>Systematic review studies have suggested that improving surveillance systems is critical in the prevention of HAIs and in reducing the emergence of antimicrobial-resistant pathogens (<xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B21">21</xref>). Therefore, a holistic approach is needed to investigate the types of disease agents, hosts, the antimicrobial-resistance profile of the organism, and the virulence of the organisms associated with HAIs in veterinary medicine (<xref ref-type="bibr" rid="B17">17</xref>).</p>
<p>This study describes the occurrence and antimicrobial-susceptibility profiles of bacterial organisms associated with HAIs and zoonosis in veterinary medicine. It addresses the following research questions: (1) Which bacteria associated with HAIs and zoonotic diseases have been reported in veterinary hospitals? (2) What are the antimicrobial resistance profiles of these bacteria?</p>
</sec>
<sec id="s2">
<title>2. Materials and methods</title>
<p>The systematic literature review was conducted using the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines (<xref ref-type="bibr" rid="B22">22</xref>). Keywords and synonyms used in various databases included hospital-acquired organism or infection, nosocomial organism or infection, animal to animal infections, zoonotic infection, zoonosis, animal to human infections, veterinary hospital, and veterinary clinic.</p>
<sec>
<title>2.1. Information source</title>
<p>Search terms and electronic databases used in this study are provided in <xref ref-type="table" rid="T1">Table 1</xref>. Since each database has a different search function, alternate search terms appropriate for each database were used. Boolean operators were utilized in all searches. A data search was conducted between June 2020 and December 2020. A follow-up search was performed in January 2021, however, there were no additional studies considered based on the inclusion criteria. Mendeley reference manager was used to store all studies and documents retrieved.</p>
<table-wrap position="float" id="T1">
<label>Table 1</label>
<caption><p>Search terms and databases utilized to search for articles included in this review about hospital-acquired and/or zoonotic infections in veterinary facilities between 2000 and 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Publications</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Search terms</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Science Direct</td>
<td valign="top" align="left">Veterinary AND &#x0201C;Infection Control&#x0201D; AND &#x0201C;hospital acquired infection OR nosocomial&#x0201D; AND zoonoses OR zoonotic OR zoonosis</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Veterinary hospital OR clinic&#x0201D; AND &#x0201C;hospital acquired infections&#x0201D; OR nosocomial AND zoonoses OR zoonotic OR zoonosis</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Systematic literature review&#x0201D; AND &#x0201C;Hospital acquired infection OR nosocomial&#x0201D; AND &#x0201C;zoonoses OR zoonosis OR zoonotic&#x0201D; AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infection OR nosocomial&#x0201D; AND &#x0201C;zoonoses OR zoonosis OR zoonotic&#x0201D; AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">Veterinary AND &#x0201C;hospital acquired infection OR nosocomial&#x0201D;</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Veterinary hospital&#x0201D; AND &#x0201C;hospital acquired infection OR nosocomial&#x0201D; NOT &#x0201C;Human hospital&#x0201D;</td>
</tr> <tr>
<td valign="top" align="left">PubMed</td>
<td valign="top" align="left">&#x0201C;Hospital acquired infections OR nosocomial&#x0201D; AND veterinary AND &#x0201C;zoonosis or zoonoses or zoonotic&#x0201D;</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Infection prevention and control&#x0201D; [All Fields] AND veterinary AND &#x0201C;hospital acquired infection or nosocomial&#x0201D; AND zoonoses</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infections OR nosocomial&#x0201D; AND veterinary</td>
</tr> <tr>
<td valign="top" align="left">Web of Science</td>
<td valign="top" align="left">&#x0201C;Hospital acquired infections&#x0201D; AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infections&#x0201D; AND &#x0201C;veterinary hospital&#x0201D;</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infections&#x0201D; AND &#x0201C;zoonotic infections&#x0201D; AND &#x0201C;Veterinary hospital&#x0201D;</td>
</tr> <tr>
<td valign="top" align="left">Google Scholar</td>
<td valign="top" align="left">&#x0201C;Systematic literature review&#x0201D; AND &#x0201C;Hospital acquired infection OR nosocomial&#x0201D; AND &#x0201C;zoonoses OR zoonosis OR zoonotic&#x0201D; AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infection OR nosocomial&#x0201D; AND &#x0201C;zoonoses OR zoonosis OR zoonotic&#x0201D; AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">&#x0201C;Hospital acquired infection OR nosocomial&#x0201D; AND &#x0201C;veterinary hospital&#x0201D;</td>
</tr> <tr>
<td valign="top" align="left">Scopus</td>
<td valign="top" align="left">&#x0201C;Hospital acquired infection&#x0201D; AND zoonoses AND veterinary</td>
</tr> <tr>
<td/>
<td valign="top" align="left">Nosocomial AND zoonoses AND veterinary</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec>
<title>2.2. Eligibility criteria</title>
<p>Only manuscripts published in peer-reviewed journals were considered for inclusion in this study. Primary research articles written in English and published between 2000 and 2020 were selected. The microbiological data included bacterial isolates from HAI cases, hospital environmental screening, fomites from veterinary hospitals, and zoonotic cases in veterinary hospitals. In addition, the antimicrobial resistance profiles of the different bacteria were also extracted. The inclusion and exclusion criteria are listed in <xref ref-type="table" rid="T2">Table 2</xref>. Two investigators (DC, DN) independently screened the titles and abstracts from the searches. Any disagreements were settled by discussion. The use of either the CLSI or EUCAST guidelines was not considered an eligibility criterion in this study since some studies report potential discrepancies between the results of the antimicrobial resistance based on CLSI and EUCAST (<xref ref-type="bibr" rid="B23">23</xref>), while others report comparable antibiotic susceptibility rates between CLSI and EUCAST breakpoints (<xref ref-type="bibr" rid="B24">24</xref>, <xref ref-type="bibr" rid="B25">25</xref>).</p>
<table-wrap position="float" id="T2">
<label>Table 2</label>
<caption><p>Inclusion and exclusion criteria of articles reporting on hospital-acquired and/or zoonotic infections in veterinary facilities between 2000 and 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Inclusion criteria</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Exclusion criteria</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Veterinary medicine studies</td>
<td valign="top" align="left">Human hospital studies</td>
</tr> <tr>
<td valign="top" align="left">Small animal/Companion animal<break/> Equine/Large animals</td>
<td valign="top" align="left">Farms, home studies</td>
</tr> <tr>
<td valign="top" align="left">Peer-reviewed research</td>
<td valign="top" align="left">Reviews</td>
</tr> <tr>
<td valign="top" align="left">Year 2000&#x02013;2020</td>
<td valign="top" align="left">Policies, Government documents and conference reports, Book chapters</td>
</tr> <tr>
<td valign="top" align="left">Studies in English</td>
<td valign="top" align="left">Non-English studies</td>
</tr> <tr>
<td valign="top" align="left">Infection prevention and control practices</td>
<td/>
</tr> <tr>
<td valign="top" align="left">(Environmental screening)</td>
<td/>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec>
<title>2.3. Study selection and data items</title>
<p>For each study that met the selection criteria for inclusion, the following data were extracted: author, year, the theme of study (HAIs or zoonotic studies), and the antimicrobial resistance profile.</p>
</sec>
</sec>
<sec id="s3">
<title>3. Results</title>
<sec>
<title>3.1. Study selection</title>
<p>Initially a total of 628 studies were identified. After initial screening, 330 articles remained. Based on the eligibility screening criteria, 48 studies remained and were further critically assessed. A total of 27 studies met the inclusion criteria and were further analyzed (<xref ref-type="fig" rid="F1">Figure 1</xref>).</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p>Summary of study selection and exclusion using the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines.</p></caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fvets-09-1087052-g0001.tif"/>
</fig>
</sec>
<sec>
<title>3.2. Risk of bias</title>
<p>Strengthening the Reporting of Observational Studies in Epidemiology (STROBE-Vet) statement is a 22-item tool that allows a systematic way of reporting on veterinary observational studies. The STROBE statement was developed to guide the reporting of observational studies related to human health. These methods have been adopted and used for standardized reporting guidelines for observational studies in veterinary medicine (<xref ref-type="bibr" rid="B21">21</xref>, <xref ref-type="bibr" rid="B26">26</xref>). Identified studies that met the inclusion criteria were cross-sectional and cohort studies (<xref ref-type="bibr" rid="B26">26</xref>). Each study was assessed individually according to each of the 22 items.</p>
<p>Items were considered to have been reported sufficiently if the studies provided a detailed abstract and clear title (item one), background, and rationale (item two), stated the objectives (item three), presented key elements of the study design (item four), described the sample size (item 11), reported outcomes for the study (items 14 and 15), provided estimates and parameters (item 16), summarized key results regarding study objectives (item 18 and 19), interpreted results (item 20), discussed the results (item 21), and stated the funding source as well as the role of authors as described by Sergeant et al. (<xref ref-type="bibr" rid="B26">26</xref>).</p>
<p>Only two studies (7%, 2/27) reported on all STROBE-Vet items (<xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B28">28</xref>). Based on STROBE-Vet, item 1 was partially attained by 19/27 (70%) studies as they excluded the study design and was fully attained by 8 (29%) studies. Items 6, 13,14, and 20 were fully attained by all the studies, Items 2, 4, 5, and 16 were fully attained by 26 (96%) of the studies, items 3,15,17, and were fully attained by 25 (93%) of the studies, item 7 and 18 were fully attained by 24 (89%) of the studies, items 9 and 19 were fully attained by 21 (78%) of the studies, items 11 and 21 were fully attained by 20 (74%) studies and item 10 was fully attained by 63% of the studies. Twelve (12; 44%) studies provided the funding sources, twelve (12; 44%) studies declared no conflict of interest, three studies (3; 11%) mentioned the contribution of each author, and three (3, 11%) provided ethical clearance declarations (<xref ref-type="supplementary-material" rid="SM1">Annexure A</xref>).</p>
</sec>
<sec>
<title>3.3. Sources of data</title>
<p>All the studies reviewed were observational. More than half (18; 67%) of the reported studies were cross-sectional studies, three (11%) were case-controlled studies (reported following an outbreak), and six (22%) were retrospective studies.</p>
<p>Twenty-four (89%) studies focused on a specific bacterium, whereas the other three studies (11%) (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B30">30</xref>) reported generally on the bacteria associated with HAIs. Most studies (78%) (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B30">30</xref>&#x02013;<xref ref-type="bibr" rid="B47">47</xref>) investigated the occurrence of HAIs in a single facility, five (19%) (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B27">27</xref>&#x02013;<xref ref-type="bibr" rid="B29">29</xref>) studies investigated multiple facilities in an area, and one (4%) (<xref ref-type="bibr" rid="B48">48</xref>) study did not specify the area of study.</p>
<p>Seventeen (17/27, 63%) studies were from either the small animal or companion animal clinics/hospitals (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B27">27</xref>&#x02013;<xref ref-type="bibr" rid="B33">33</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B41">41</xref>&#x02013;<xref ref-type="bibr" rid="B44">44</xref>, <xref ref-type="bibr" rid="B48">48</xref>). followed by both bovine (<xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B49">49</xref>, <xref ref-type="bibr" rid="B50">50</xref>) (4/27, 15%) and equine medicine (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>). Three (3/27, 11%) studies were a combination of small animals, large animals, and poultry (<xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B40">40</xref>). One (1/27, 4 %) study did not identify the type of veterinary clinic or hospital (<xref ref-type="bibr" rid="B39">39</xref>).</p>
<p>Within the hospital settings, bacteria associated with HAIs were reported from environmental surfaces (9/27; 33%) (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B44">44</xref>, <xref ref-type="bibr" rid="B47">47</xref>), animal cases (8/27; 30%) (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B33">33</xref>, <xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B43">43</xref>, <xref ref-type="bibr" rid="B47">47</xref>), and commonly used fomites such as clothing, cell phones, clippers, stethoscopes, and computers (4/27, 15%) (<xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B41">41</xref>). Only three studies (3/27, 11%) isolated bacteria from humans who have regular contact with animals (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B38">38</xref>).</p>
<p>The antimicrobial resistance profile of the different organisms was provided in eighteen (17/27, 63%) studies (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B33">33</xref>&#x02013;<xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>, <xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>), while nine (9/27, 33%) studies did not report on the antimicrobial resistance patterns (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B41">41</xref>, <xref ref-type="bibr" rid="B44">44</xref>, <xref ref-type="bibr" rid="B48">48</xref>). Thirteen studies (13/27, 48%) further characterized the microorganisms using pulsed-field gel electrophoresis (PFGE) and polymerase chain reaction (PCR) assays (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B33">33</xref>&#x02013;<xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B45">45</xref>&#x02013;<xref ref-type="bibr" rid="B47">47</xref>).</p>
</sec>
<sec>
<title>3.4. Bacterial species associated with hospital-acquired infections</title>
<p><italic>Staphylococcus</italic> spp. were the most (17/27, 63%) reported pathogens associated with HAIs, followed by <italic>Escherichia coli</italic> (5/27; 19%), <italic>Enterococcus</italic> spp. (4/27; 15%)<italic>, Salmonella</italic> spp. (4/27; 15%), <italic>A. baumannii</italic> (4/27; 15%), <italic>C. difficile</italic> (1/27; 4%), and <italic>P. aeruginosa</italic>. (1/27; 4%). <italic>Enterococcus faecalis</italic> (3/4; 75%) and <italic>E. faecium</italic> (3/4; 75%) were the most reported among the <italic>Enterococcus</italic> species.</p>
<p>Among the <italic>Staphylococcus</italic> spp., 11 (11/17, 65%) were MRSA and six (6/17, 35%) were methicillin-resistant <italic>S. pseudintermedius</italic> (MRSP). Three out of five (3/5; 60%) studies reported MDR <italic>Escherichia coli</italic> isolates and one (1/5; 20%) study reported an extended spectrum &#x003B2;-lactamase (ESBL) producing <italic>E. coli</italic>. Meanwhile, vancomycin-resistant <italic>enterococci</italic> were reported in one (1/4; 25%) study. <italic>Salmonella</italic> Typhimurium was reported as the common serotype in two of the four (2/4; 50%) studies. The other two of the four (2/4; 50%) studies reported the presence of MDR <italic>Salmonella</italic> (<xref ref-type="table" rid="T3">Table 3</xref>).</p>
<table-wrap position="float" id="T3">
<label>Table 3</label>
<caption><p>Organism reported in hospital-acquired and/or zoonotic infections in veterinary facilities between 2000 and 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Bacteria</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Citation</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left"><italic>Staphylococcus</italic> spp.</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B32">32</xref>&#x02013;<xref ref-type="bibr" rid="B34">34</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B40">40</xref>&#x02013;<xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B44">44</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Methicillin-resistant <italic>S. aureus</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B35">35</xref>&#x02013;<xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B41">41</xref>, <xref ref-type="bibr" rid="B51">51</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Methicillin-resistant <italic>S. pseudintermedius</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B41">41</xref>, <xref ref-type="bibr" rid="B44">44</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Clostridium difficile</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Enterococcus</italic> spp.</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>E. faecalis</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>E. faecium</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Vancomycin-resistant enterococci</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Acinetobacter baumannii</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B39">39</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Escherichia coli</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B50">50</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Extended spectrum &#x003B2;-lactamase (ESBL)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Multidrug resistance <italic>E. coli</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B39">39</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Salmonella</italic> spp.</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Multidrug-resistant <italic>Salmonella</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Pseudomonas aeruginosa</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec>
<title>3.5. Sources of organisms associated with hospital-acquired infections</title>
<p>The following pathogens were detected in the hospital environmental surfaces, namely MRSA (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B40">40</xref>), MRSP (<xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B44">44</xref>), ESBL-producing <italic>E. coli</italic> isolates (<xref ref-type="bibr" rid="B17">17</xref>), VRE (<xref ref-type="bibr" rid="B17">17</xref>), <italic>A. baumannii</italic> (<xref ref-type="bibr" rid="B39">39</xref>), <italic>C. difficile</italic> (<xref ref-type="bibr" rid="B17">17</xref>) and <italic>P. aeruginosa</italic> (<xref ref-type="bibr" rid="B42">42</xref>). Common pathogens identified from hospital fomites included: MRSA (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B41">41</xref>), MRSP (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B41">41</xref>), <italic>Enterococcus faecalis</italic> (<xref ref-type="bibr" rid="B42">42</xref>), and <italic>A. baumannii</italic> (<xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B39">39</xref>).</p>
<p>Among patients in hospital settings, MRSA was isolated from companions (<xref ref-type="bibr" rid="B35">35</xref>) and equine animals (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B34">34</xref>). Multidrug resistant <italic>Escherichia coli</italic> was isolated from companion and bovine animals (<xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B50">50</xref>). Additionally, <italic>Enterococcus faecium, Enterococcus faecalis</italic> (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B46">46</xref>) and <italic>A. baumannii</italic> (<xref ref-type="bibr" rid="B3">3</xref>) were isolated from companion animals. <italic>Salmonella</italic> species were also isolated from patients (<xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B47">47</xref>), healthy animals (<xref ref-type="bibr" rid="B46">46</xref>), and the hospital environment (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B46">46</xref>) (<xref ref-type="table" rid="T4">Table 4</xref>).</p>
<table-wrap position="float" id="T4">
<label>Table 4</label>
<caption><p>Sources of hospital acquired organisms based on the systematic reviewed papers published from 2000 to 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Source</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><xref ref-type="table-fn" rid="TN1"><sup>a</sup></xref>MRSA</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><xref ref-type="table-fn" rid="TN2"><sup>b</sup></xref>MRSP</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><xref ref-type="table-fn" rid="TN3"><sup>c</sup></xref>ESBL E. coli</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><xref ref-type="table-fn" rid="TN4"><sup>d</sup></xref>MDR</bold><break/> <bold><italic>Escherichia coli</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>Enterococcus faecalis</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>Enterococcus faecium</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>C. difficile</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>P. aeruginosa</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>A. baumannii</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>Salmonella</italic> spp</bold>.</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" colspan="11" style="background-color:#e0e1e3"><bold>Animal</bold></td>
</tr> <tr>
<td valign="top" align="left">Patients</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B35">35</xref>)<break/> (<xref ref-type="bibr" rid="B34">34</xref>)<break/> (<xref ref-type="bibr" rid="B19">19</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B31">31</xref>)<break/> (<xref ref-type="bibr" rid="B50">50</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B3">3</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B47">47</xref>)<break/> (<xref ref-type="bibr" rid="B38">38</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Healthy</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)</td>
</tr> <tr>
<td valign="top" align="left" colspan="11" style="background-color:#e0e1e3"><bold>Environment</bold></td>
</tr> <tr>
<td valign="top" align="left">Hospital</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B40">40</xref>)<break/> (<xref ref-type="bibr" rid="B37">37</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B44">44</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)</td>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B39">39</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)<break/> (<xref ref-type="bibr" rid="B46">46</xref>)</td>
</tr> <tr>
<td valign="top" align="left">Equipment</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B19">19</xref>)<break/> (<xref ref-type="bibr" rid="B36">36</xref>)<break/> (<xref ref-type="bibr" rid="B32">32</xref>)<break/> (<xref ref-type="bibr" rid="B41">41</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>)<break/> (<xref ref-type="bibr" rid="B9">9</xref>)<break/> (<xref ref-type="bibr" rid="B41">41</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B29">29</xref>)<break/> (<xref ref-type="bibr" rid="B32">32</xref>)<break/> (<xref ref-type="bibr" rid="B39">39</xref>)</td>
<td/>
</tr> <tr>
<td valign="top" align="left">Healthcare workers</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B52">52</xref>)<break/> (<xref ref-type="bibr" rid="B27">27</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B32">32</xref>)</td>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left">Pet Owners</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B27">27</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B34">34</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="TN1"><p><sup>a</sup>MRSA, Methicillin-resistant <italic>Staphylococcus aureus</italic>.</p></fn>
<fn id="TN2"><p><sup>b</sup>MRSP, Methicillin-resistant <italic>Staphylococcus pseudintermediu</italic>s.</p></fn>
<fn id="TN3"><p><sup>c</sup>ESBL-<italic>E. coli</italic>, Extended-spectrum beta-lactamase producing- <italic>E. coli</italic>.</p></fn>
<fn id="TN4"><p><sup>d</sup>MDR-<italic>E. coli</italic>, Multidrug-resistant <italic>E. coli</italic>.</p></fn>
</table-wrap-foot>
</table-wrap>
<p>The healthcare workers (HCWs) harbored MRSA (<xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B42">42</xref>), MRSP (<xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B42">42</xref>), <italic>E. faecium</italic> (<xref ref-type="bibr" rid="B42">42</xref>) and two studies reported MRSA among pet owners (<xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B34">34</xref>). In addition, van Duijkeren et al. (<xref ref-type="bibr" rid="B35">35</xref>) and Hoet et al. (<xref ref-type="bibr" rid="B20">20</xref>) reported on the zoonotic potential of MRSA with van Duijkeren (<xref ref-type="bibr" rid="B35">35</xref>) identifying MRSA clusters in animals with a similar clonal lineage to that reported in humans (<bold>Table 6</bold>).</p>
</sec>
<sec>
<title>3.6. Antimicrobial resistance patterns of bacteria associated with hospital acquired infections</title>
<sec>
<title>3.6.1. Phenotypic resistance</title>
<p>Out of the 27 studies reviewed, 17 (63%) conducted an antimicrobial susceptibility test on the isolates. Among these, 12 (71%) studies reported isolates resistant to more than one antimicrobial. Bacteria resistant to multiple drugs identified included MRSA (<xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B34">34</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B45">45</xref>), MRSP (<xref ref-type="bibr" rid="B42">42</xref>), <italic>A. baumannii</italic> (<xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B39">39</xref>), <italic>E. coli</italic> (<xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B48">48</xref>), <italic>Salmonella</italic> Typhimurium (<xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>), <italic>E. faecalis</italic> and <italic>E. faecium</italic> (<xref ref-type="bibr" rid="B43">43</xref>).</p>
<p>Methicillin-resistant <italic>Staphylococcus aureus</italic> isolates showed resistance toward ampicillin, amoxicillin, oxacillin, clindamycin, gentamycin, ciprofloxacin, cephalexin, enrofloxacin, cefuroxime, chloramphenicol, erythromycin, and kanamycin while MRSP isolates showed resistance toward azithromycin, oxacillin, penicillin, clindamycin, gentamycin, tetracycline, and ciprofloxacin. <italic>Clostridioides difficile</italic> showed resistance toward rifampin, moxifloxacin, and chloramphenicol. <italic>Enterococcus faecalis</italic> and <italic>E. faecium</italic> showed resistance toward ampicillin, tetracycline, ciprofloxacin, enrofloxacin, erythromycin, and rifampicin (<xref ref-type="bibr" rid="B43">43</xref>). <italic>Enterococcus faecium</italic> was also reported to be resistant to amoxicillin and vancomycin (<xref ref-type="bibr" rid="B42">42</xref>).</p>
<p><italic>Acinetobacter baumannii</italic> exhibited resistance to amoxicillin, tetracycline (<xref ref-type="bibr" rid="B39">39</xref>), ciprofloxacin (<xref ref-type="bibr" rid="B28">28</xref>) and imipenem (<xref ref-type="bibr" rid="B28">28</xref>). While <italic>E. coli</italic> showed resistance to ampicillin, cefoxitin, oxacillin, and penicillin (<xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B48">48</xref>) and <italic>Salmonella</italic> was resistant to ampicillin, amoxicillin, cefoxitin, gentamycin, tetracycline, chloramphenicol, rifampicin, and streptomycin (<xref ref-type="bibr" rid="B47">47</xref>) (<xref ref-type="table" rid="T5">Table 5</xref>).</p>
<table-wrap position="float" id="T5">
<label>Table 5</label>
<caption><p>Phenotypic antimicrobial resistance profile of hospital-acquired infection organisms based on the systematically reviewed papers published from 2000 to 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Pathogens</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>AMP</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>AMX</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CEF</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>AZI</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>OXA</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>PEN</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CLI</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>GEN</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>TET</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CIP </bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>VAN</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CFL</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>ENF</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CFR</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CHL</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>ERY</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>KAN</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>RIF</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>MOX</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CLO</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>CPH</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>IMI</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>STR</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>AMX-C</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left" colspan="25" style="background-color:#e0e1e3"><bold>Gram-positive bacteria</bold></td>
</tr> <tr>
<td valign="top" align="left"><xref ref-type="table-fn" rid="TN5"><sup>a</sup></xref>MRSA</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B35">35</xref>)<xref ref-type="table-fn" rid="TN7"><sup>&#x0002A;</sup></xref><break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B40">40</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)<break/> (<xref ref-type="bibr" rid="B35">35</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B40">40</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B38">38</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B40">40</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B40">40</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B37">37</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B35">35</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B35">35</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)<break/> (<xref ref-type="bibr" rid="B35">35</xref>)<break/> (<xref ref-type="bibr" rid="B20">20</xref>)<break/> (<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B37">37</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><xref ref-type="table-fn" rid="TN6"><sup>b</sup></xref>MRSP</td>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><italic>E. faecium</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)<break/> (<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B40">40</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><italic>E. faecalis</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B40">40</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><italic>C. difficile</italic></td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B19">19</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B19">19</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B19">19</xref>)</td>
<td/>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left" colspan="25" style="background-color:#e0e1e3"><bold>Gram-negative bacteria</bold></td>
</tr> <tr>
<td valign="top" align="left"><italic>E. coli</italic></td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B48">48</xref>)<break/> (<xref ref-type="bibr" rid="B31">31</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B48">48</xref>)<break/> (<xref ref-type="bibr" rid="B31">31</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B48">48</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B48">48</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B50">50</xref>)<break/> (<xref ref-type="bibr" rid="B33">33</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>A. baumannii</italic></td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B39">39</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B39">39</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B28">28</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B28">28</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B28">28</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B19">19</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B28">28</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Salmonella spp</italic>.</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td/>
<td/>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B46">46</xref>)<break/> (<xref ref-type="bibr" rid="B47">47</xref>)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>AMP, Ampicillin; AMX, Amoxicillin; CEF, Cefoxitin; AMX-C, Amoxycillin-Clavulanic Acid; AZI, Azithromycin; OXA, Oxacillin; PEN, Penicillin; CLI, Clindamycin; GEN, Gentamicin; TET, Tetracycline; CIP, Ciprofloxacin; VAN, Vancomycin; LIN, Linezolid; CFL, Cephalexin; ENF, Enrofloxacin; CFR, Cefuroxime; CHL, Chloramphenicol; ERY, Erythromycin; KAN, Kanamycin; CHL, Chloramphenicol; STR, Streptomycin; RIF, Rifampin; IMI, Imipenem; MOX, Moxifloxacin; CLO, Clarithromycin; IMI, Imipenem; STR, Streptomycin.</p>
<fn id="TN5"><p><sup>a</sup>MRSA, Methicillin-resistant <italic>Staphylococcus aureus</italic>.</p></fn>
<fn id="TN6"><p><sup>b</sup>MRSP, Methicillin-resistant <italic>Staphylococcus pseudintermedius</italic>.</p></fn>
<fn id="TN7"><p><sup>&#x0002A;</sup>References in the brackets correspond to studies that have reported resistance to the antimicrobials.</p></fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec>
<title>3.6.2. Antimicrobial genes</title>
<p>Among <italic>Staphylococcus</italic> species, <italic>mec</italic>A was reported in five MRSA studies (<xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B49">49</xref>) and two MRSP studies (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B42">42</xref>). &#x003B2;-lactamase gene (<italic>bla</italic><sub>CMY &#x02212; 2</sub> gene) was reported in <italic>Salmonella</italic> spp. (<xref ref-type="bibr" rid="B47">47</xref>) and <italic>E. coli</italic> isolates (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B48">48</xref>). While the vancomycin-resistant gene (<italic>van</italic>A gene) was reported by one <italic>E. faecium</italic> study (<xref ref-type="bibr" rid="B42">42</xref>). The <italic>flo</italic> gene was identified in one <italic>E. coli</italic> study (<xref ref-type="bibr" rid="B31">31</xref>) (<xref ref-type="table" rid="T6">Table 6</xref>).</p>
<table-wrap position="float" id="T6">
<label>Table 6</label>
<caption><p>The antimicrobial resistant genes isolated from bacteria associated with hospital-acquired infections data published between 2000 and 2020.</p></caption>
<table frame="box" rules="all">
<thead><tr>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold>Pathogens</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>mec</italic>A</bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>bla</italic><sub>CMY &#x02212; 2</sub></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>flo</italic></bold></th>
<th valign="top" align="left" style="background-color:#919497; color:#ffffff"><bold><italic>van</italic>A</bold></th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left"><xref ref-type="table-fn" rid="TN8"><sup>a</sup></xref>MRSA</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B49">49</xref>)<xref ref-type="table-fn" rid="TN10"><sup>&#x0002A;</sup></xref></td>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><xref ref-type="table-fn" rid="TN9"><sup>b</sup></xref>MRSP</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B42">42</xref>)</td>
<td/>
<td/>
<td/>
</tr> <tr>
<td valign="top" align="left"><italic>E. coli</italic></td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B48">48</xref>)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B31">31</xref>)</td>
<td/>
</tr> <tr>
<td valign="top" align="left"><italic>E. faecium</italic></td>
<td/>
<td/>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B42">42</xref>)</td>
</tr> <tr>
<td valign="top" align="left"><italic>Salmonella</italic> spp.</td>
<td/>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td/>
<td/>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="TN8"><p><sup>a</sup>MRSA, Methicillin-resistant <italic>Staphylococcus aureus</italic>.</p></fn>
<fn id="TN9"><p><sup>b</sup>MRSP, Methicillin-resistant <italic>Staphylococcus pseudintermedius</italic>.</p></fn>
<fn id="TN10"><p><sup>&#x0002A;</sup>References in the brackets correspond to studies that have reported resistance to the antimicrobials.</p></fn>
</table-wrap-foot>
</table-wrap>
</sec>
</sec>
<sec>
<title>3.7. Zoonotic diseases</title>
<p>Six (22%) studies (<xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B34">34</xref>, <xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B45">45</xref>, <xref ref-type="bibr" rid="B50">50</xref>) reported organisms associated with HAIs that are zoonotic in nature. For example, MRSA with a SCC<italic>mec</italic> type IV isolated in humans (<xref ref-type="bibr" rid="B28">28</xref>) has also been isolated in hospitalized horses (<xref ref-type="bibr" rid="B45">45</xref>) and hospitalized dogs (<xref ref-type="bibr" rid="B40">40</xref>). Similarly, three studies reported clonal MRSA lineage in animals similar to that previously reported in humans (<xref ref-type="bibr" rid="B34">34</xref>, <xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B40">40</xref>). The plasmid DH108/30218 from <italic>E. coli</italic> isolates which is similar to a cassette (18-ESBL 188) reported in humans (<xref ref-type="bibr" rid="B50">50</xref>) has been identified.</p>
</sec>
</sec>
<sec id="s4">
<title>4. Discussion</title>
<p>Hospital-acquired infections and zoonosis are increasingly becoming a global concern (<xref ref-type="bibr" rid="B53">53</xref>). In addition, there is an increasing prevalence of resistance among these organisms to commonly used antimicrobials. Most studies that have investigated HAIs and their antimicrobial resistance profiles are in human medicine. In view of this, studies on the occurrence and resistant profile of organisms associated with hospital-acquired and zoonotic infections in veterinary medicine are needed. In this study, bacterial organisms associated with hospital-acquired and zoonotic infections isolated were identified. Furthermore, most of the organisms identified were multidrug-resistant or harbored resistant genes. Several sources of bacterial organisms associated with HAIs including HCWs, commonly used instruments, fomites, and contaminated hospital environments were also identified.</p>
<sec>
<title>4.1. Hospital-acquired bacterial infections</title>
<p>Bacteria associated with HAIs identified MRSA, MRSP, <italic>Enterococcus</italic> spp., <italic>A. baumannii, P. aeruginosa, C. difficile, E. coli</italic>, and <italic>Salmonella</italic> spp., (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B30">30</xref>). The presence of these bacterial pathogens within veterinary settings is a public health concern and emphasizes the need for the implementation of infection prevention and control measures to eliminate these pathogens. The patient microbiota, healthcare workers, fomites, and the hospital environment were identified as possible sources of organisms associated with HAIs. Therefore, control measures being implemented should be source-specific and moment-specific during patient care (<xref ref-type="bibr" rid="B54">54</xref>).</p>
<sec>
<title>4.1.1. Sources of bacterial organisms associated with hospital acquired infections</title>
<p>Identification of sources of organisms associated with HAIs in veterinary settings is critical to reducing the risk of transmission to patients and humans. Therefore, it is not surprising that most studies have largely focused on the hospital environment and commonly used instruments as potential reservoirs for organisms associated with HAIs (<xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B41">41</xref>, <xref ref-type="bibr" rid="B44">44</xref>). Furthermore, there are ongoing epidemiological studies to understand the relationship between environmental cleanliness and the risk of transmission of HAIs in veterinary settings (<xref ref-type="bibr" rid="B4">4</xref>).</p>
<p>The intensive care unit (ICU), surgical ward, in-house laboratory, and consultation rooms were the most important environmental sources of bacteria associated with HAIs in veterinary hospitals (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B42">42</xref>). Furthermore, environmental surfaces with human contact tend to have higher contamination levels compared to those without human contact (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B42">42</xref>), suggesting that humans may play a major role in the transmission of these organisms within the hospital environment. This is further emphasized by studies that have isolated similar pathogens strains from the environment and hands of HCWs (<xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B47">47</xref>, <xref ref-type="bibr" rid="B53">53</xref>). Therefore, HCWs in veterinary hospitals must be trained on hand hygiene compliance to reduce the risk of transmission of HAI organisms.</p>
<p>Fomites served as sources of HAI organisms and facilitated transmission between animal patients, the hospital environment, and humans (<xref ref-type="bibr" rid="B32">32</xref>). Fomites such as clippers, personnel clothing (<xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B39">39</xref>), cell phones (<xref ref-type="bibr" rid="B41">41</xref>), stethoscopes (<xref ref-type="bibr" rid="B39">39</xref>), and weighing scales (<xref ref-type="bibr" rid="B39">39</xref>) were reported to be contaminated with bacteria associated with HAIs. Therefore, the development and implementation of cleaning and disinfection protocols to prevent transmission is needed (<xref ref-type="bibr" rid="B2">2</xref>). In addition, all surgical materials, instruments, and other fomites which increase the possibility of transmission of these organisms must be sterilized before use (<xref ref-type="bibr" rid="B36">36</xref>).</p>
</sec>
<sec>
<title>4.1.2. Methicillin-resistant <italic>Staphylococcus aureus</italic></title>
<p>Methicillin-resistant <italic>Staphylococcus aureus</italic> was among the most common organism associated with HAIs in this study (<xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B37">37</xref>). The organisms were reported in wound infection (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B35">35</xref>), invasive procedures (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B35">35</xref>), skin infections (<xref ref-type="bibr" rid="B34">34</xref>), asymptomatic animals (<xref ref-type="bibr" rid="B45">45</xref>), septic arthritis, pneumonia, incisional site infection, and rhinitis (<xref ref-type="bibr" rid="B19">19</xref>). Studies done in veterinary medicine also reported <italic>Staphylococcus</italic> strains similar to those reported in humans were reported in this study (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B45">45</xref>). For example, Loeffler et al. (<xref ref-type="bibr" rid="B27">27</xref>) in the UK identified MRSA clones (CC22 and CC30) among humans working with or in close proximity to animals suggesting transmission between animals and humans is precise (<xref ref-type="bibr" rid="B37">37</xref>).</p>
<p>Unhygienic environmental conditions are a major source of MRSA (<xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B44">44</xref>). Therefore, implementing effective infection prevention and control (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B52">52</xref>) and screening animals before hospitalization will reduce the spread of MRSA in veterinary hospitals. This is likely to reduce costs associated with increased length of hospital stay (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B27">27</xref>, <xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B45">45</xref>).</p>
<p>Most MRSA isolates in this study were resistant to &#x003B2;-lactam, 2nd generation cephalosporins, lincosamides, and aminoglycosides. While one study reported intermediate susceptibility to vancomycin among MRSA isolates (<xref ref-type="bibr" rid="B36">36</xref>). The presence of vancomycin resistance is concerning as it is the last resort for the treatment of MRSA in humans. Similarly, the presence of &#x003B2;-lactam resistance among staphylococci facilitated by the <italic>mec</italic>A gene (<xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B35">35</xref>&#x02013;<xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B49">49</xref>) is likely to contribute to resistance to other antimicrobials with a &#x003B2;-lactam ring (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B45">45</xref>). Therefore, the implementation and constant review of infection control protocols are needed to help reduce the risk of the transfer of resistance genes to other organisms (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B55">55</xref>&#x02013;<xref ref-type="bibr" rid="B57">57</xref>). Without these interventions, patient care and treatment will likely be negatively impacted (<xref ref-type="bibr" rid="B36">36</xref>, <xref ref-type="bibr" rid="B40">40</xref>).</p>
</sec>
<sec>
<title>4.1.3. Methicillin-resistant <italic>Staphylococcus pseudintermedius</italic></title>
<p>Methicillin-resistant <italic>Staphylococcus pseudintermedius</italic> like MRSA has emerged as a leading cause of opportunistic infections in companion animals (<xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B42">42</xref>). The organism has been reported in asymptomatic animals, implant-associated surgical sites (<xref ref-type="bibr" rid="B41">41</xref>), fomites (<xref ref-type="bibr" rid="B9">9</xref>, <xref ref-type="bibr" rid="B32">32</xref>, <xref ref-type="bibr" rid="B41">41</xref>), and in the environment within the veterinary hospital (<xref ref-type="bibr" rid="B44">44</xref>). Therefore, colonized, and contaminated areas remain potential sources of hospital-acquired infections (<xref ref-type="bibr" rid="B32">32</xref>).</p>
<p>Areas in the veterinary facilities have been shown to harbor MRSP. These include surfaces such as tables, chairs, floors, and surgical environments (<xref ref-type="bibr" rid="B58">58</xref>&#x02013;<xref ref-type="bibr" rid="B60">60</xref>). Moreover, some MRSP organisms are able to survive cleaning and disinfection (<xref ref-type="bibr" rid="B58">58</xref>, <xref ref-type="bibr" rid="B59">59</xref>). In view of the potential resistance to disinfectants coupled with ineffective cleaning, these areas can become a source of infection for susceptible animals. Notwithstanding, some disinfectants if used at the correct concentrations are effective against MRSP (<xref ref-type="bibr" rid="B61">61</xref>, <xref ref-type="bibr" rid="B62">62</xref>).</p>
<p>Of concern is that MRSP is highly resistant to antimicrobials commonly used for the treatment of <italic>S. pseudintermedius</italic> infections (<xref ref-type="bibr" rid="B63">63</xref>&#x02013;<xref ref-type="bibr" rid="B65">65</xref>). These organisms have been isolated from the environment and hands of HCWs (<xref ref-type="bibr" rid="B42">42</xref>), which is concerning as it limits treatment options. Similar to MRSA, MRSP can acquire the <italic>mec</italic>A gene (<xref ref-type="bibr" rid="B42">42</xref>). Shoen et al. (<xref ref-type="bibr" rid="B9">9</xref>) showed coagulase positive <italic>S. pseudintermedius</italic> commonly isolated from the skin of dogs can acquire the <italic>mec</italic>A gene from a coagulase-negative <italic>S. epidermidis</italic> commonly found in humans.</p>
<p>The zoonotic cases associated with MRSP are not common (<xref ref-type="bibr" rid="B32">32</xref>). However, an MRSA spa type 18/t338 from animal-related fomites has been reported in humans (<xref ref-type="bibr" rid="B41">41</xref>). The rise in the number of MRSP cases between dogs, pet owners, and veterinary staff is concerning, therefore, effective hand hygiene should be performed before and after contact with the patient, as well as after contact with potentially contaminated environmental sites within veterinary hospitals.</p>
</sec>
<sec>
<title>4.1.4. <italic>Enterococcus</italic> species</title>
<p><italic>Enterococcus</italic> species are commensal of the gut flora of cats and dogs (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B43">43</xref>). However, they are also opportunistic pathogens (<xref ref-type="bibr" rid="B3">3</xref>). In recent years, <italic>Enterococcus</italic> species have emerged as causes of HAIs in veterinary medicine associated with urinary tract infections (UTIs) (<xref ref-type="bibr" rid="B66">66</xref>). The transmission is mainly due to fecal contaminated fomites or environmental surfaces (<xref ref-type="bibr" rid="B29">29</xref>). These organisms can survive in a hospital environment for a long period. Furthermore, they can survive high temperatures and disinfectants such as chlorine and alcohol (<xref ref-type="bibr" rid="B42">42</xref>).</p>
<p><italic>Enterococcus faecium</italic> and <italic>E. faecalis</italic> are the most predominant species reported in dogs (<xref ref-type="bibr" rid="B30">30</xref>, <xref ref-type="bibr" rid="B43">43</xref>), hospital environments and in hands of HCWs (<xref ref-type="bibr" rid="B42">42</xref>). Of the two species, <italic>E. faecalis</italic> is the predominant enterococci. Multidrug-resistant enterococci have also been reported as a commensal and pathogenic organism (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>). The presence of MDR among <italic>Enterococcus</italic> species has largely been attributed to overuse and misuse of antimicrobials (<xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B43">43</xref>). It is also possible that some may have acquired resistance through other mechanisms including genetic transfer or mutation (<xref ref-type="bibr" rid="B43">43</xref>). For example, resistance to erythromycin has been associated with the methylation of the ribosomal target site of these antibiotics (<xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B67">67</xref>). Nonetheless, the presence of MDR enterococci is likely to impact patient care in veterinary hospitals (<xref ref-type="bibr" rid="B42">42</xref>).</p>
<p>Of concern is the emergence of vancomycin-resistant <italic>E. faecium</italic> (<xref ref-type="bibr" rid="B42">42</xref>) which is an important antimicrobial in the treatment of enterococci infections (<xref ref-type="bibr" rid="B43">43</xref>, <xref ref-type="bibr" rid="B67">67</xref>) and is mediated by the presence of <italic>van</italic>A genes. These genes are important as they confer multidrug resistance and may be transmitted to other bacterial species such as <italic>Staphylococcus</italic> and create even bigger problems in the treatment of HAIs (<xref ref-type="bibr" rid="B42">42</xref>). Furthermore, these genes can also be transferred from animals to humans (<xref ref-type="bibr" rid="B3">3</xref>, <xref ref-type="bibr" rid="B43">43</xref>).</p>
</sec>
<sec>
<title>4.1.5. <italic>Clostridioides difficile</italic></title>
<p><italic>Clostridioides difficile</italic> is found in the hospital environmental and it is difficult to eradicate (<xref ref-type="bibr" rid="B17">17</xref>). Both humans and animals are asymptomatically carriers of the organism. In humans, its presence has been attributed to the overuse of antimicrobials. However, in veterinary medicine there is limited information about the organism. Therefore, future studies should look at whether the overuse of antimicrobials could be a driver of <italic>C. difficile</italic> in veterinary settings (<xref ref-type="bibr" rid="B17">17</xref>). The ability of the pathogen to survive harsh environmental conditions and resistance to most disinfectants makes it a suitable indicator of the effective IPC measures (<xref ref-type="bibr" rid="B17">17</xref>). Therefore, it is possible that this organism can also be used as an indicator of effective infection prevention and control in veterinary hospitals.</p>
</sec>
<sec>
<title>4.1.6. <italic>Acinetobacter baumannii</italic></title>
<p><italic>Acinetobacter baumannii</italic> causes life-threatening infections in both humans and animals. This organism has been reported in UTIs, pyothorax, upper airway obstruction, bloodstream infection, and wound infections in animals (<xref ref-type="bibr" rid="B39">39</xref>). In infected animals, it is associated with increased morbidity and prolonged length of hospital stay (<xref ref-type="bibr" rid="B68">68</xref>). <italic>Acinetobacter baumannii</italic> survives on dry surfaces (<xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B69">69</xref>). Therefore, commonly used fomites, bed rails, cages, and examination tables could serve as reservoirs for <italic>A. baumannii</italic>.</p>
<p>The organism can survive stressful environmental conditions and remains viable on different surfaces (<xref ref-type="bibr" rid="B70">70</xref>). However, if used at correct concentrations, sodium hypochlorite (bleach) and 70% ethanol are effective against <italic>A. baumannii</italic> (<xref ref-type="bibr" rid="B70">70</xref>, <xref ref-type="bibr" rid="B71">71</xref>). Lanjri et al. (<xref ref-type="bibr" rid="B71">71</xref>) observed that chlorhexidine digluconate was effective against <italic>A. baumannii</italic>. La Forgia et al. (<xref ref-type="bibr" rid="B72">72</xref>) also reported that sodium hypochlorite was effective in reducing the incidence rate of <italic>A. baumannii</italic> in hospital settings. In light of this findings, choosing the correct disinfectant is important in reducing cases of <italic>A. baumannii</italic> in hospital settings.</p>
<p>Most <italic>A. baumannii</italic> are multiple drug resistant with a high prevalence of resistance toward cephalexin, enrofloxacin, amoxicillin-clavulanic acid, sulphamethoxazole-trimethoprim, and tetracycline (<xref ref-type="bibr" rid="B39">39</xref>). Resistance to the above antimicrobials is concerning as these antimicrobials are commonly used for the treatment of bacterial infections in small animal medicine (<xref ref-type="bibr" rid="B68">68</xref>). In addition, the <italic>bla</italic>OXA-51 gene reported in an <italic>A. baumannii</italic> isolate from pigs has also been reported in humans (<xref ref-type="bibr" rid="B67">67</xref>).</p>
</sec>
<sec>
<title>4.1.7. <italic>Escherichia coli</italic></title>
<p><italic>Escherichia coli</italic> is commonly reported in UTIs and bloodstream infections (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B73">73</xref>). The bacterium spreads from patient to patient <italic>via</italic> fecal contaminated hands of HCWs and shared equipment (<xref ref-type="bibr" rid="B31">31</xref>). Given, that environmental surfaces could potentially be a reservoir of <italic>E. coli</italic>, measures to minimize fecal contamination in companion animal hospitals including cleaning and disinfection of the hospital environment should be implemented. Moreover, Sanchez et al. (<xref ref-type="bibr" rid="B31">31</xref>) shows the transfer of <italic>E. coli</italic> isolates with similar antimicrobial resistance patterns between two different animals admitted to the same ICU.</p>
<p>In this study, <italic>E. coli</italic> isolates exhibited resistance toward cephalosporins and &#x003B2;-lactams including amoxycillin-clavulanic acid. This broad-spectrum antimicrobial resistance among <italic>E. coli</italic> is attributed to the presence of <italic>amp</italic>C like gene, <italic>bla</italic><sub>CMY2</sub> (<xref ref-type="bibr" rid="B17">17</xref>, <xref ref-type="bibr" rid="B31">31</xref>), which has been identified to be of public health concern (<xref ref-type="bibr" rid="B17">17</xref>). Another study reported resistance among <italic>E. coli</italic> isolates to chloramphenicol mainly due to the presence of <italic>cml</italic>A homologue <italic>flo</italic> among gram-negative bacteria (<xref ref-type="bibr" rid="B31">31</xref>). The presence of these genes has also been linked to the development of resistance to other commonly used antibiotics such as gentamycin, spectinomycin, and sulfadimethoxine (<xref ref-type="bibr" rid="B31">31</xref>, <xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B50">50</xref>). Considering this resistance, strict guidelines should be implemented on the prudent use of antimicrobials in veterinary medicine.</p>
</sec>
<sec>
<title>4.1.8. <italic>Salmonella</italic> species</title>
<p>Although most animals are asymptomatic carriers of <italic>Salmonella</italic> spp., they shed the bacterium in high quantities through their feces resulting in <italic>Salmonella</italic> outbreaks in equine veterinary hospitals (<xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>). Furthermore, infections associated with <italic>Salmonella</italic> species have also been reported in bovine with diarrhea, fever, dehydration (<xref ref-type="bibr" rid="B38">38</xref>) and colic in horses (<xref ref-type="bibr" rid="B47">47</xref>). In affected animals, the disease is characterized by high morbidity and mortality. There is a potential spread of organisms and the occurrence of zoonotic infection that may result in the closure of facilities and a loss of income for the hospital (<xref ref-type="bibr" rid="B38">38</xref>, <xref ref-type="bibr" rid="B46">46</xref>). Therefore, personnel working in close contact with infected animals are at an increased risk of infection (<xref ref-type="bibr" rid="B46">46</xref>).</p>
<p>Managing transmission in the veterinary settings remains a challenge as <italic>Salmonella</italic> can persist in the environment for a long time. Rodents and contaminated feed could also be a source (<xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>). Therefore, biosecurity measures must be intensified in veterinary hospitals to reduce the risk of transmission. Additionally, education programs can also be developed targeting specific aspects of hygiene, movement control, and cleanliness of equipment.</p>
<p><italic>Salmonella</italic> isolates were resistant to ceftiofur, gentamycin, amoxicillin, ampicillin, streptomycin, and trimethoprim/ sulfadiazine (<xref ref-type="bibr" rid="B46">46</xref>, <xref ref-type="bibr" rid="B47">47</xref>). One study reported the presence of the cephalomycinase gene, <italic>bla</italic><sub>cmy2</sub> (<xref ref-type="bibr" rid="B47">47</xref>) which has been associated with cephalosporin resistance among <italic>Salmonella</italic> species. This gene has also been reported to mediate resistance to amoxicillin, amoxicillin-clavulanic acid, cephalothin, cefoxitin, ceftiofur, and ceftriaxone (<xref ref-type="bibr" rid="B47">47</xref>).</p>
</sec>
</sec>
</sec>
<sec id="s5">
<title>5. Conclusion</title>
<p>Organisms associated with hospital-acquired and zoonotic diseases were reported from clinical cases, environmental surfaces, and items used in veterinary service. The hospital environment with human contact was the most reported source of organisms associated with HAIs. These results suggest that humans play a crucial role in the transmission of HAIs in veterinary hospitals.</p>
<p>Among the organisms reported, MRSA <italic>and</italic> MRSP were the most reported HAI organisms in veterinary facilities. Other organisms identified include <italic>E. coli, C. difficile, A. baumannii, Salmonella</italic> spp., and <italic>Enterococcus</italic> species. Some of these isolates reported in veterinary settings share similar clonal lineage to those reported in humans. Some organisms exhibit a high prevalence of antimicrobial resistance and contain genes known to be associated with antibiotic resistance.</p>
<p>These results suggest that strict infection prevention and control practices must be in place, monitored and modified when necessary to curb the occurrence and transmission of organisms associated with HAIs in veterinary hospitals. In addition, continuous surveillance of HAI organisms and their antimicrobial resistance patterns in veterinary hospitals should be emphasized. Further research needs to be done on <italic>C. difficile</italic> as a potential indicator of effective infection prevention and control practices in veterinary facilities.</p>
</sec>
<sec sec-type="data-availability" id="s6">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/<xref ref-type="sec" rid="s9">Supplementary material</xref>, further inquiries can be directed to the corresponding authors.</p>
</sec>
<sec sec-type="author-contributions" id="s7">
<title>Author contributions</title>
<p>DS was involved in study design, data analysis, interpretation of results, and writing of manuscript as well as extensive editing of the manuscript. DQ was involved in study design, data management, analysis, and interpretation as well as reviewing of the manuscript draft. JO and MK were involved in study design, data analysis, and interpretation as well as editing of the manuscript. All authors have read and approved the final manuscript.</p>
</sec>
</body>
<back>
<ack><p>The authors would like to extend their appreciation to the National Research Foundation for providing the scholarship funding.</p>
</ack>
<sec sec-type="COI-statement" id="conf1">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec sec-type="disclaimer" id="s8">
<title>Publisher&#x00027;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
<sec sec-type="supplementary-material" id="s9">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fvets.2022.1087052/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fvets.2022.1087052/full#supplementary-material</ext-link></p>
<supplementary-material xlink:href="Table_1.DOCX" id="SM1" mimetype="application/vnd.openxmlformats-officedocument.wordprocessingml.document" xmlns:xlink="http://www.w3.org/1999/xlink"/>
</sec>
<ref-list>
<title>References</title>
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