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Brief report
Molecular subtyping of Salmonella spp. strains in provincial abattoirs with no hazard analysis critical control point from Buenos Aires, Argentina
Subtipificación molecular de Salmonella spp. en frigoríficos provinciales sin análisis de peligros y puntos críticos de control ubicados en Buenos Aires, Argentina
Magdalena Costa
Corresponding author
mcosta@igevet.gob.ar

Corresponding author.
, Victoria Brusa, Alejandra Londero, Lucía Galli, Gerardo A. Leotta
IGEVET – Instituto de Genética Veterinaria “Ing. Fernando N. Dulout” (UNLP-CONICET LA PLATA), Facultad de Ciencias Veterinarias, Av. 60 y 118 s/n, CC: 296 UNLP (1900), La Plata, Buenos Aires, Argentina
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0020" class="elsevierStylePara elsevierViewall">Salmonellosis represents an important public health concern worldwide&#44; with an estimated 93&#46;8 million gastroenteritis cases and 155&#44;000 deaths annually due to <span class="elsevierStyleItalic">Salmonella</span> species&#44; of which 85&#46;6&#37; are foodborne&#46; Human salmonellosis has been associated with contaminated food products&#44; primarily those of animal origin&#44; as well as with direct contact with infected animals<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a>&#46; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; contaminate meat in the abattoir during slaughter by spreading from the hide and the intestinal tract of animals&#46; Moreover&#44; knives&#44; workers&#44; platforms and equipment can become sources of cross contamination<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Argentine bovine abattoirs are classified into exporter&#44; federal transit and provincial transit<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#44; and have different hygiene and sanitation standards&#46; Provincial transit abattoirs do not always have a Hazard Analysis Critical Control Point &#40;HACCP&#41; system&#59; although they comply with the sanitary requirements of each provincial health authority&#44; they do not implement the microbiological verification of either product or the environment<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46; Thus&#44; meeting the zero tolerance criteria for <span class="elsevierStyleItalic">Salmonella</span> is quite difficult in abattoirs with no HACCP system&#46; In our country&#44; characterization and subtyping studies of this bacterial group in bovine abattoirs have not been previously conducted&#46; For this reason&#44; knowledge about circulating <span class="elsevierStyleItalic">Salmonella</span> spp&#46; clones in this environment is scarce&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">We have previously demonstrated that the prevalence of <span class="elsevierStyleItalic">Salmonella enterica</span> in products&#44; by-products and environmental samples can be reduced by implementing improvement actions and food handlers&#8217; training<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46; The aim of the present work was to characterize <span class="elsevierStyleItalic">S&#46; enterica</span> isolates by pulsed-field gel electrophoresis &#40;PFGE&#41; in order to establish their epidemiological relationships&#44; contamination routes and spread in abattoirs&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">We subtyped 32 <span class="elsevierStyleItalic">Salmonella enterica</span> strains previously isolated from three provincial abattoirs with no HACCP system from Buenos Aires&#44; Argentina during 2016&#8211;2018<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46; For that purpose&#44; the provincial health authority selected three licensed abattoirs &#40;identified as A&#44; B and C&#41; located at less than 100<span class="elsevierStyleHsp" style=""></span>km from the sample processing laboratory&#44; each of them with an average slaughter of 150&#8211;200 animals per day<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Samplings included carcasses &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>252&#41;&#44; the environment &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>252&#44; involving workers&#8217; hands&#44; knives&#44; workers&#8217; boots&#44; platforms&#44; cool chambers and bathroom&#41;&#44; head meat &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#41; and viscera washing and chilling water &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>105&#44; involving heart&#44; sweetbread&#44; liver&#44; kidney and chitterlings&#41;&#46; Isolation of <span class="elsevierStyleItalic">Salmonella</span> spp&#46; was carried out according to ISO 6579-1&#58;2017<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">6</span></a>&#46; In the baseline study<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#44; 26 strains were isolated in 2016 before implementing improvement actions &#40;stage I&#59; 10 samplings per establishment&#41;&#44; and other six strains were isolated in 2018 after their implementation &#40;stage III&#59; 4 samplings per establishment&#41;&#44; although it was not possible to implement an HACCP plan<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; strains were isolated from carcasses &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>10&#41;&#44; the environment &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; head meat &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; and viscera washing and chilling water &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#41;&#46; The strains belonged to six serovars&#58; Anatum &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; Montevideo &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>12&#41;&#44; Typhimurium &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; Give &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; Cerro &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; and Newport &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; <a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">For the PFGE analysis&#44; the one-day &#40;24&#8211;26<span class="elsevierStyleHsp" style=""></span>h&#41; PulseNet standardized laboratory protocol<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">4</span></a> for molecular subtyping of <span class="elsevierStyleItalic">Salmonella</span> serotypes was employed&#46; Restriction digestion of DNA in agarose plugs was carried out with the <span class="elsevierStyleItalic">Xba</span>I enzyme &#40;Thermo Scientific&#44; MA&#44; USA&#41;&#46; MaestroGen slider imager &#40;Maestrogen Inc&#46;&#44; Nevada&#44; USA&#41; was used to obtain PFGE images of the gels&#46; Tagged file format &#40;TIFF&#41; image analysis was conducted using the BioNumerics version 6&#46;6 software package &#40;Applied Maths&#44; Sint-Martens-Latem&#44; Belgium&#41; using the Dice coefficient and the unweighted pair group method with arithmetic mean &#40;UPGMA&#41; to generate dendrograms with 1&#46;5&#37; band matching tolerance&#46; Two or more isolates were grouped into a cluster when they shared an identical pattern &#40;100&#37; similarity&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">A dendrogram with 10 restriction patterns with at least 51&#46;8&#37; similarity was obtained&#46; Five unique patterns and five clusters were obtained &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Isolates from serovar Anatum showed four patterns &#40;two corresponding to unique strains and the other two in more than one isolate&#41; with at least 87&#46;4&#37; similarity&#46; Cluster I included four isolates from abattoir A obtained from carcasses &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41; and workers&#8217; boots &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; on sampling 2&#44; and carcass &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; on sampling 7&#46; These findings would indicate cross-contamination by direct contact with carcasses&#59; persistence of contamination for more than a month in the abattoir environment would become a possible source of environmental contamination<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Cluster II included eight strains of serovar Anatum&#44; from the three abattoirs studied&#46; In abattoir A&#44; one strain was isolated from workers&#8217; boots in 2016 and another from sweetbread washing and cooling water in 2018&#46; The ability of <span class="elsevierStyleItalic">S</span>&#46; anatum to persist in the environment for years has already been described by Carlson et al<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">3</span></a>&#46; On this basis&#44; we hypothesized that the strains were circulating&#44; persisted in the animals and contaminated the establishment at different times with the same clone&#44; or that the strains persisted in the abattoir environment&#46; In abattoir B&#44; two strains were isolated from workers&#8217; hands on different samplings&#46; In abattoir C&#44; four clonal isolates were obtained from three different carcasses and workers&#8217; boots on the same sampling&#46; This highlighted the importance of reinforcing good hygiene practices &#40;GHP&#41;&#44; since workers would be a possible source of contamination of the final product<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a>&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">S&#46;</span> Montevideo serovars &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>12&#41; were grouped into the same cluster &#40;III&#41; with at least 96&#46;8&#37; similarity&#44; except for one strain from abattoir C that gave a unique pattern&#46; In abattoir B&#44; the strains were isolated from carcasses&#44; workers&#8217; hands and knives on sampling 7&#59; from workers&#8217; hands&#44; boots and liver washing and cooling water on sampling 8&#59; from workers&#8217; hands on sampling 9&#44; and from sweetbread washing and cooling water on sampling 10&#46; The presence of clones for more than one month evidenced the capacity of <span class="elsevierStyleItalic">S&#46;</span> Montevideo to persist in the environment<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">3</span></a>&#46; Additionally&#44; the same clone was isolated from workers&#8217; hands during three consecutive samplings&#44; showing its persistence among workers&#44; thus entailing an additional risk&#44; namely&#44; the propagation of these strains in and out of the abattoir&#46; In abattoir A&#44; the strain was isolated from platforms on two successive samplings &#40;2 and 3&#41; and from chitterling washing and cooling water on sampling 3&#44; indicating the lack of correct sanitation standard operating procedures<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Contrary to what was described by other authors<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">1&#44;9&#44;11</span></a>&#44; isolates from serovars Typhimurium&#44; Give&#44; Cerro and Newport were circumstantial in short periods of time&#46; Cluster IV grouped two <span class="elsevierStyleItalic">S&#46;</span> Typhimurium isolates from carcasses and head meat in abattoir A on the same sampling&#44; probably due to the low capacity of this serovar to form biofilms and persist<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a>&#46; Two clonal strains of serovar Give were also isolated from workers&#8217; hands and carcasses in the mentioned abattoir on two successive samplings &#40;cluster V&#41;&#46; Although this serovar has been associated with cattle in the province of Buenos Aires<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a>&#44; its detection in workers&#8217; hands represented a source of contamination in the establishment<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a>&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The results obtained revealed the simultaneous presence of different clones of <span class="elsevierStyleItalic">S&#46; enterica</span> serovars in the same abattoir by <span class="elsevierStyleItalic">Xba</span>I-PFGE&#44; as well as their self-perpetuating capacity&#46; However&#44; these strains should be analyzed using genome sequencing-based methods such as whole genome sequencing<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a> to obtain more robust conclusions&#46; In the meantime&#44; provincial abattoirs from Argentina should be strictly monitored and&#44; besides promoting GHP&#44; the implementation of an HACCP plan is necessary to meet the zero-tolerance criteria for <span class="elsevierStyleItalic">Salmonella</span> on beef&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Funding</span><p id="par0075" class="elsevierStylePara elsevierViewall">This research did not receive any specific grant from funding agencies in the public&#44; commercial or not-for-profit sectors&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Conflicts of interest</span><p id="par0080" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Salmonella enterica</span> was established in products and the environment&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Cross-contamination in abattoirs was confirmed&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">The application of HACCP is necessary to meet the zero-tolerance criteria for <span class="elsevierStyleItalic">Salmonella</span> on beef&#46;</p></li></ul></p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We subtyped 32 <span class="elsevierStyleItalic">Salmonella enterica</span> strains isolated from carcasses &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>10&#41;&#44; the environment &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; head meat &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; and viscera washing and chilling water &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#41; in provincial abattoirs with no Hazard Analysis Critical Control Point &#40;HACCP&#41; system from Buenos Aires&#44; Argentina&#44; before and after implementing improvement actions&#46; Pulsed-field gel electrophoresis &#40;PFGE&#41; was carried out using the <span class="elsevierStyleItalic">Xba</span>I restriction enzyme&#46; Strains belonged to six serovars&#44; from which 10 restriction patterns were obtained &#40;five unique patterns and five clusters&#41;&#46; We found different clones of <span class="elsevierStyleItalic">S&#46; enterica</span> serovars in the same abattoir by <span class="elsevierStyleItalic">Xba</span>I-PFGE&#46; In addition to promoting good hygiene practices&#44; the implementation of an HACCP plan is necessary to meet the zero-tolerance criteria for <span class="elsevierStyleItalic">Salmonella</span> on beef&#46;</p></span>"
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        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Subtipificamos en total 32 cepas de <span class="elsevierStyleItalic">Salmonella enterica</span> aisladas de carcasas &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>10&#41;&#44; medio ambiente &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; carne de cabeza &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; y agua de lavado y enfriamiento de v&#237;sceras &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#41; en frigor&#237;ficos provinciales de Buenos Aires &#40;Argentina&#41; sin an&#225;lisis de peligros y puntos cr&#237;ticos de control &#40;<span class="elsevierStyleItalic">hazard analysis critical control point</span> &#91;HACCP&#93;&#41;&#59; la toma de muestras se efectu&#243; antes y despu&#233;s de implementar acciones de mejora&#46; Se llev&#243; a cabo electroforesis en gel de campo pulsado &#40;PFGE&#41; utilizando la enzima de restricci&#243;n <span class="elsevierStyleItalic">Xba</span>I&#46; Las cepas pertenec&#237;an a 6 serovares y presentaron 10 patrones de restricci&#243;n &#40;5 patrones &#250;nicos y 5 <span class="elsevierStyleItalic">clusters</span>&#41;&#46; Demostramos la presencia de diferentes serovares de <span class="elsevierStyleItalic">S&#46; enterica</span> en un mismo frigor&#237;fico mediante <span class="elsevierStyleItalic">Xba</span>I-PFGE&#46; Adem&#225;s de las buenas pr&#225;cticas de higiene&#44; se requiere la aplicaci&#243;n de un HACCP para cumplir con los criterios de tolerancia cero para <span class="elsevierStyleItalic">Salmonella</span> en carne bovina&#46;</p></span>"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">XbaI-PFGE dendrogram&#44; strain number&#44; sample type&#44; serovar&#44; abattoir&#44; stage&#44; sampling and sampling date of <span class="elsevierStyleItalic">Salmonella enterica</span> strain isolates &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>32&#41; from three Argentine abattoirs&#46;</p>"
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ISSN: 03257541
Original language: English
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