Antimicrobial Resistance Profiles of the Two Porcine Salmonella Typhimurium Isolates

Year 2016, Volume: 42 Issue: 2, 156 - 160, 04.07.2016

Kemal Metiner , Özden Büyükbaba Boral Baran Çelik , Belgi Diren Sığırcı , Beren Başaran Kahraman , Seyyal Ak

https://doi.org/10.16988/iuvfd.2016.43290

Abstract

The aim of the study is to detect the presence of the Salmonella species in swine with diarrhea, and to investigate their antimicrobial resistance and extended spectrum beta lactamase (ESBL) and/or AmpC β-lactamase production. For this purpose, stool samples from three commercial pig farms in Istanbul and Tekirdag were collected and processed for Salmonella isolation by culture and isolates were identified by biochemical activity tests. Salmonella isolates were confirmed by PCR then serotyped. Antimicrobial resistance and ESBL and AmpC production of the isolates were determined according to the Clinical and Laboratory Standards Institute (CLSI) standard. In the study, two hundred and thirty eight stool samples were examined. Salmonella spp. were obtained from 2 samples, and the isolation rate was determined as 0.8%. Both of the isolates were defined as Salmonella enterica subsp. enterica serovar Typhimurium (serotype 1, 4, [5], 12: I: 1, 2) by serotyping. Both of them were resistant to cefaclor, cloxacillin and lincomycin (100%). Multidrug resistance (resistance ≥3 antimicrobials) observed in all isolates. ESBL and AmpC production were not detected in any of the isolates. To our knowledge, this is the first report of the isolation of S. Typhimurium in pigs with diarrhea in Turkey. This study also represents the first report of multi-drug resistant S. Typhimurium isolates from pig stools in Turkey.

References

• Arias, C.A., Murray, B.E., 2015. A new antibiotic and the evolution of resistance. New England Journal of Medicine 372, 1168-1170.
• Aydın, F., Umur, Ç., Gökçe, G., Genç, O., Güler, M.A., 2001. The isolation and identification of bacteria and parasites from diarrhoeic calves in Kars District. Journal of the Faculty of Veterinary Medicine, Kafkas University 7, 7-14.
• Bağcıgil, A.F., İkiz, S., Metiner, K., Özgür, N.Y., Ak, S., Ilgaz, A.A., 2013. Isolation of Streptococcus species from the tonsils of slaughtered pigs. Turkish Journal of Veterinary and Animal Sciences 37, 94-96.
• Bagcigil, F.A., Moodley, A., Baptiste, K.E., Jensen, V.F., Guardabassi, L., 2007. Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Veterinary Microbiology 121, 307-315.
• Baggesen, D.L., Sandvang, D., Aarestrup, F.M., 2000. Characterization of Salmonella enterica Salmonella enterica serovar Typhimurium DT104 isolated from Denmark and comparison with isolates from Europe and the United States. Journal of Clinical Microbiology 38, 1581-1586.
• Bolton, D.J., Ivory, C., McDowell, D., 2013. A study of Salmonella in pigs from birth to carcass: serotypes, genotypes, antibiotic resistance and virulence profiles. International Journal of Food Microbiology 160, 298-303.
• Boyen, F., Haesebrouck, F., Maes, D., van Immerseel, F., Ducatelle, R., Pasmans, F., 2008. Non-typhoidal Salmonella infections in pigs: A closer look at epidemiology, pathogenesis and control. Veterinary Microbiology 130, 1-19.
• CLSI (Clinical and Laboratory Standards Institute), 2013. M100-S23-performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. CLSI, Wayne, Pennsylvania.
• Davies, R., 2004. Salmonellosis. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. OIE, World Organization for Animal Health, 1018-1032.
• de Jong, A., Smet, A., Ludwig, C., Stephan, B., De Graef, E., Vanrobaeys, M., Haesebrouck, F., 2014. Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008–2011). Veterinary Microbiology 171, 298-306.
• EFSA (European Food Safety Authority), 2011. Scientific opinion on the public health risks of bacterial strains producing extended-spectrum β-lactamases and/or ampc β-lactamases in food and food-producing animals. EFSA Panel on Biological Hazards (BIOHAZ). EFSA Journal 9, 2322, 1-95.
• Erdem, B., Ercis, S., Hascelik, G., Gur, D., Gedikoglu, S., Aysev, A.D., Sumerkan, B., Tatman-Otkun, M., Tuncer, I., 2005. Antimicrobial resistance patterns and serotype distribution among Salmonella enterica strains in Turkey, 2000-2002. European Journal of Clinical Microbiology and Infectious Diseases 24, 220-225.
• Ertaş, N., Al, S., Karadal, F., Gönülalan, Z., 2014. Kayseri İlinde Satışa Sunulan Manda Yoğurtlarının Mikrobiyolojik Kalitesi. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 40, 83-89.
• Frye, J.G., Fedorka-Cray, P.J., 2007. Prevalence, distribution and characterisation of ceftiofur resistance in Salmonella enterica isolated from animals in the USA from 1999 to 2003. International Journal of Antimicrobial Agents 30, 134-142.
• Genç, O., 2002. The isolation, identification and serotyping of Salmonella isolated from domestic animals in Kars district. Journal of the Faculty of Veterinary Medicine, Kafkas University 8, 23-30
• Genç, O., Otlu, S., 2005. Salmonella isolations from different avian species in Kars district of Turkey. The Journal of the Faculty of Veterinary Medicine, Kafkas University 11, 25-27.
• Giske, C.G., Martinez-Martinez, L., Cantón, R., Stefani, S., Skov, R., Glupczynski, Y., Poland, M.G., 2012. EUCAST Guidelines for Detection of Resistance Mechanisms and Specific Resistances of Clinical and/or Epidemiological Importance. European Commitee on Antimicrobial Susceptibility Testing, 1-47.
• Holt, J.G., Krieg, N.R., Sneath, P.H.A., Staley, J.T., Williams, S.T., 1994. Bergey’s Manual of Determinative Bacteriology, Ninth Edition. Lippincott Williams and Wilkins, USA.
• Li, R., Lai, J., Wang, Y., Liu, S., Li, Y., Liu, K., Shen, J., Wu, C., 2013. Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China. International Journal of Food Microbiology 163, 14-18.
• Li, X.Z., Mehrotra, M., Ghimire, S., Adewoye, L., 2007. βLactam resistance and β-lactamases in bacteria of animal origin. Veterinary Microbiology 121, 197-214.
• Metiner, K., Ak, S., 2007. Presence and seroprevalence of Actinobacillus pleuropneumoniae in pigs in Turkey. Acta Veterinaria Brno 76, 237-244.
• Metiner, K., Anğ Küçüker, M., Büyükbaba Boral, Ö., Anğ, Ö., 2013. First isolation of Enterococcus strains in pig faeces in Turkey and determination of antibiotic susceptibilities. Acta Veterinaria Brno 82, 231-235.
• Mmolawa, P.T., Willmore, R., Thomas, C.J., Heuzenroeder, M.W., 2002. Temperate phages in Salmonella enterica serovar Typhimurium: Implications for epidemiology. International Journal of Medical Microbiology 291,633-644.
• Poppe, C., Ziebell, K., Martin, L., Allen, K., 2004. Diversity in Antimicrobial Resistance and Other Characteristics Among Salmonella Typhimurium DT104 Isolates. Microbial Drug Resistance 8, 107-122.
• Rahn, K., De Grandis, S.A., Clarke, R.C., McEwen, S.A., Galán, J.E., Ginocchio, C., Curtiss III, R., Gyles, C.L., 1992. Amplification of an invA gene sequence of Salmonella Typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and Cellular Probes 6, 271-279.
• Rajić, A., McFall, M.E., Deckert, A.E., Reid-Smith, R., Manninen, K., Poppe, C., Dewey, C.E., McEwen, S.A., 2004. Antimicrobial resistance of Salmonella isolated from finishing swine and the environment of 60 Alberta swine farms. Veterinary Microbiology 104, 189-196.
• Rice, D.H., Hancock, D.D., Roozen, P.M., Szymanski, M.H., Scheenstra, B.C., Cady, K.M., Besser, T.E., Chudek, P.A., 2003. Household Contamination with Salmonella enterica. Emerging Infectious Diseases 9, 120-122.
• Shanmugasamy, M., Velayutham, T., Rajeswar, J., 2011. InvA gene specific PCR for detection of Salmonella from broilers. Veterinary World 4, 562-564.
• Sisak, F., Havlickova, H., Hradecka, H., Rychlik, I., Kolackova, I., Karpiskova, R., 2006. Antibiotic resistance of Salmonella spp. isolates from pigs in the Czech Republic. Veterinarni Medicina 51, 303–310.
• Swanenburg, M., Berends, B.R., Urlings, H.A.P., Snijders, J.M.A., van Knapen, F., 2001. Epidemiological investigations into the sources of Salmonella contamination of pork. Berliner und Münchener Tierarztliche Wochenschrift 114, 356-359.
• Türkyılmaz, S., Savaşan, S., Kırkan, Ş., Kaya, O., 2007. Detection of Salmonella Enteritidis infections in poultry by using bacteriological and serological methods. Journal of the Faculty of Veterinary Medicine Istanbul University 33, 23-33.
• Van Boxstael, S., Dierick, K., Van Huffel, X., Uyttendaele, M., Berkvens, D., Herman, L., Bertrand, S., Wildemauwe, C., Catry, B., Butaye, P., Imberechts, H., 2012. Comparison of antimicrobial resistance patterns and phage types of Salmonella Typhimurium isolated from pigs, pork and humans in Belgium between 2001 and 2006. Food Research International 45, 913-918.
• Van den Brandhof, W.E., van Pelt, W., Wagenaar, J.A., van Duynhoven, Y.T.H.P., 2003. Study on the sources of human campylobacteriosis and salmonellosis in the Netherlands. Infectieziekten Bulletin 14, 132-135.
• Van Pelt, W., de Wit, M.A.S., Wannet, W.J.B., Ligtvoet, E.J.J., Widdowson, M.A., van Duynhoven, Y.T.H.P., 2003. Laboratory surveillance of bacterial gastroenteric pathogens in The Netherlands, 1991–2001. Epidemiology and Infection 130, 431-441.
• Vieira-Pinto, M., Tenreiro, R., Martins, C., 2006. Unveiling contamination sources and dissemination routes of Salmonella sp. in pigs at a Portuguese slaughterhouse through macrorestriction profiling by pulsed-field gel electrophoresis. International Journal of Food Microbiology 110, 77-84.
• White, D.G., Zhao, S., Singh, R., McDermoot, P.F., 2004. Antimicrobial Resistance Among Gram-Negative Foodborne Bacterial Pathogens Associated with Foods of Animal Origin. Foodborne Pathogens and Disease 1,137-152.
• Wright, J.G., Tengelsen, L.A., Smith, K.E., Bender, J.B., Frank, R.K., Grendon, J.H., Rice, D.H., Thiessen, A.M.B., Gilbertson, C.J., Sivapalasingam, S., Barret, T.J., Besser, T.E., Hancock, D.D., Angulo, F.J., 2005. Multidrug-resistant Salmonella Typhimurium in Four Animal Facilities. Emerging Infectious Diseases 11,1235-1241.
• Yılmaz, M.A., Aslantaş, Ö., Özer, B., Yılmaz, E.Ş., 2015. Nasal Carriage of Methicillin-Resistant Coagulase Negative Staphylococci (MR-CoNS) Among Veterinarians and Veterinary Students. Journal of the Faculty of Veterinary Medicine Istanbul University 41, 69-78.