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Salmonella enterica subsp. enterica isolated from chicken carcasses and environment at slaughter in Reunion Island: prevalence, genetic characterization and antibiotic susceptibility

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A Publisher’s Erratum to this article was published on 22 February 2014

Abstract

Salmonella contamination of 71 chicken broiler flocks was investigated at the slaughterhouse in Reunion Island between October 2007 and January 2009. Samples were collected from live broiler chickens and chicken carcasses as well as the slaughterhouse environment. Salmonella spp. was isolated from 40 of 71 (56 % with a confidence interval 5 % [45–67]) broiler chicken flocks at slaughter. The most prominent serovars were Blockley (31 %), Typhimurium and Brancaster (14 %), Hadar (10 %), Salmonella multidrug resistant clinical organisms serotypes 1,4,[5],12:i:-, and Virchow (8 %) and Livingstone, St. Paul, Seftenberg, Llandoff, Infantis and Indiana. At the farm, 27 % of the broiler chicken flocks tested positive for Salmonella spp. Salmonella spp. was isolated from 124 of 497 environmental samples (25 %). In most cases, there was no relationship between pulsed field gel electrophoresis (PFGE) pattern and antibiotic resistance pattern. The predominant Salmonella serovars were susceptible to most of the tested antibiotic drugs, but S. Hadar exhibited multidrug resistance. This study highlighted the primary source of Salmonella was the farm of origin and downstream stages in processing could not remedy to but amplify this Salmonella contamination.

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References

  • Achen, M., Morishita, T. Y. and Ley, E. C., 1998. Shedding and colonization of Campylobacter jejuni in broilers from day-of-hatch to slaughter age. Avian Diseases 42, 732-737.

    Article  PubMed  CAS  Google Scholar 

  • Arsenault, J., Letellier, A., Quessy, S. and Boulianne, M., 2007. Prevalence and risk factors for Salmonella and Campylobacter spp. carcass contamination in broiler chickens slaughtered in Quebec, Canada. Journal of Food Protection 70, 1820-1828.

    PubMed  Google Scholar 

  • Arumugaswamy, R. K., Rusul, G., Hamid, S. N. A. and Cheah, C. T., 1995. Prevalence of Salmonella in raw and cokeed foods in Malaysia. Food Microbiology 12, 3-8.

    Article  Google Scholar 

  • Baggesen, D. L., Wingstrand, A., Carstensen, B., Nielsen, B. and Aarestrup, F. M., 1999. Effects of the antimicrobial growth promoter tylosin on subclinical infection of pigs with Salmonella enterica serotype typhimurium. American Journal of Veterinary Research 60, 1201-1206.

    PubMed  CAS  Google Scholar 

  • Beli, E., Duraku, E. and Telo, A., 2001. Salmonella serotypes isolated from chicken meat in Albania. International Journal of Food Microbiology 71, 263-266.

    Article  PubMed  CAS  Google Scholar 

  • Breuil, J., Brisabois, A., Casin, I., Armand_Lefevre, L., Fremy, S. and Collatz, E., 2000. Antibiotic resistance in salmonellae isolated from humans and animals in France: comparative data from 1994 and 1997. The Journal of Antimicrobial Chemotherapy 46, 965-971.

    Article  PubMed  CAS  Google Scholar 

  • Cardinale, E., Tall, F., Gueye, E. F., Cisse, M. and Salvat, G., 2004. Risk Factors for Salmonella enterica subsp. enterica infection in Senegalese broiler-chicken flocks. Preventive Veterinary Medicine In Press.

  • Cason, J. A., Hinton, A. and Ingram, K. D., 2000. Coliform, Escherichia coli, and salmonellae concentrations in a multiple-tank, counterflow poultry scalder. Journal of Food Protection 63, 1184-1188.

    PubMed  CAS  Google Scholar 

  • D’Aoust, J. Y., 1989. Salmonella. In: M. P. Doyle (Ed.), Foodborne bacterial pathogens. Marcel Dekker Inc., New York, pp. 327 - 446.

    Google Scholar 

  • D’ortenzio, E., Weill, F., Ragonneau, S., Lebon, J.A., Renault, P., Pierre, V. 2008. First report of a Salmonella enterica servovar Weltevreden outbreak on Reunion Island, France, August 2007. Euro surveillance 13, 393-395.

    Google Scholar 

  • David, J. M., Danan, C., Chauvin, C., Chazel, M., Souillard, R., Brisabois, A., Weill, F. X., Jourdan-Da Silva, N., Picherot, M., Guillemot, D. and Sanders, P., 2011. Structure of the French farm-to-table surveillance system for Salmonella. Revue De Medecine Veterinaire 162, 489-500.

    Google Scholar 

  • Davies, R., Breslin, M., Corry, J. E., Hudson, W. and Allen, V. M., 2001. Observations on the distribution and control of Salmonella species in two integrated broiler companies. The Veterinary Record 149, 227-232.

    Article  PubMed  CAS  Google Scholar 

  • EFSA. 2010. Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008—Part A: Campylobacter and Salmonella prevalence estimates

  • Fontin, G., Sanavio, G., Maini, C., Giugliano, I. and Polli, A. C., 1993. Isolamento di salmonelle nel triennio 1989-1991 da acque superficiali, coprocolture ed alimenti. Bollettino di Microbiologia e Indagini di Laboratorio 13, 15-24.

    Google Scholar 

  • Heyndrickx, M., Vandekerchove, D., Herman, L., Rollier, I., Grijspeerdt, K. and De_Zutter, L., 2002. Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 129, 253-265.

    Article  PubMed  CAS  Google Scholar 

  • Higgins, R., Malo, R., Rene_Roberge, E. and Gauthier, R., 1981. Studies on the dissemination of Salmonella in nine broiler-chicken flocks. Avian Diseases 26, 26-33.

    Article  Google Scholar 

  • Hue, O., Le Bouquin, S., Lalande, F., Allain, V., Rouxel, S., Petetin, I., Quesne, S., Laisney, M. J., Gloaguen, P. Y., Picherot, M., Salvat, G., Bougeard, S. and Chemaly, M., 2011. Prevalence of Salmonella spp. on broiler chicken carcasses and risk factors at the slaughterhouse in France in 2008. Food Control 22, 1158-1164.

    Article  Google Scholar 

  • Hunter, P., Erasmus, B. J. and Vorster, J. H., 2002. Teratogenicity of a mutagenised Rift Valley fever virus (MVP 12) in sheep. Onderstepoort Journal of Veterinary Research 69, 95-98.

    PubMed  CAS  Google Scholar 

  • Jorgensen, F., Bailey, R., Williams, S., Henderson, P., Wareing, D. R., Bolton, F. J., Frost, J. A., Ward, L. and Humphrey, T. J., 2002. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. International Journal of Food Microbiology 76, 151-164.

    Article  PubMed  CAS  Google Scholar 

  • Kerouanton, A., Marault, M., Lailler, R., Weill, F. X., Feurer, C., Espie, E. and Brisabois, A., 2007. Pulsed-field gel electrophoresis subtyping database for foodborne Salmonella enterica serotype discrimination. Foodborne Pathogens and Disease 4, 293-303.

    Article  PubMed  CAS  Google Scholar 

  • Kim, A., Lee, Y. J., Kang, M. S., Kwag, S. I. and Cho, J. K., 2007. Dissemination and tracking of Salmonella spp. in integrated broiler operation. Journal of Veterinary Science 8, 155-161.

    Article  PubMed  CAS  Google Scholar 

  • Lahellec, C. and Colin, P., 1985. Relationship between serotypes of Salmonellae from hatcheries and rearing farms and those from processed poultry carcases. British Poultry Science 26, 179-186.

    Article  PubMed  CAS  Google Scholar 

  • Lawson, B., Hughes, L. A., Peters, T., de Pinna, E., John, S. K., Macgregor, S. K. and Cunningham, A. A., 2011. Pulsed-field gel electrophoresis supports the presence of host-adapted Salmonella enterica subsp enterica serovar typhimurium strains in the British garden bird population. Applied and Environmental Microbiology 77, 8139-8144.

    Article  PubMed  CAS  Google Scholar 

  • Lillard, H. S., 1988. Comparison of sampling methods and implication for bacterial decontamination of poultry carcassses iby rinsing. Journal of Food Protection 51, 405-408.

    Google Scholar 

  • Limawongpranee, S., Hayashidani, H., Okatani, A. T., Ono, K., Hirota, C., Kaneko, K. and Ogawa, M., 1999. Prevalence and persistence of Salmonella in broiler chicken flocks. Journal of Veterinary Medical Science 61, 255-259.

    Article  PubMed  CAS  Google Scholar 

  • Malorny, B., Schroeter, A. and Helmuth, R., 1999. Incidence of quinolone resistance over the period 1986 to 1998 in veterinary Salmonella isolates from Germany. Antimicrobial Agents and Chemotherapy 43, 2278-2282.

    PubMed  CAS  Google Scholar 

  • Martin, S. W., Meek and P., W., 1987. Veterinary epidemiology: principles and methods. Iowa State University Press/Ames.

  • Medeiros, M. I., Neme, S. N., da_Silva, P., Capuano, D. M., Errera, M. C., Fernandes, S. A., do_Valle, G. R. and de_Avila, F. A., 2001. Etiology of acute diarrhea among children in Ribeiro Preto-SP, Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 43, 21-24.

    Article  PubMed  CAS  Google Scholar 

  • Meerburg, B. G. and Kijlstra, A., 2007. Role of rodents in transmission of Salmonella and Campylobacter. Journal of the Science of Food and Agriculture 87, 2774-2781.

    Article  CAS  Google Scholar 

  • Mellor, G. E., Duffy, L. L., Dykes, G. A. and Fegan, N., 2010. Relative prevalence of Salmonella sofia on broiler chickens pre- and postprocessing in Australia. Poultry Science 89, 1544-1548.

    Article  PubMed  CAS  Google Scholar 

  • Murugkar, H., Rahman, H., Kumar, A. and Bhattacharyya, D. 2005. Isolation, phage typing & antibiogram of Salmonella from man & animals in northeastern India. Indian Journal of Medical Research 122, 237-242.

    PubMed  CAS  Google Scholar 

  • Musgrove, M. T., Cason, J. A., Fletcher, D. L., Stern, N. J., Cox, N. A. and Bailey, J. S., 1997. Effect of cloacal plugging on microbial recovery from partially processed broilers. Poultry Science 76, 530-533.

    PubMed  CAS  Google Scholar 

  • Pacini, R., Quagli, E., Galassi, R., Tozzi, E. and Malloggi, L., 1994. Dieci anni di sorveglianza epidemiologica a Livorno (I parte) Studio epidemiologico sulle salmonelle isolate da portatori sani, nell’area livornese, dal 1984 al 1993. Bollettino di Microbiologia e Indagini di Laboratorio 14, 9-14.

    Google Scholar 

  • Padungtod, P. and Kaneene J. B., 2006. Salmonella in food animals and humans in northern Thailand. International Journal Of Food Microbiology 108, 346-354.

    Google Scholar 

  • Popoff, M. Y., Bockemuhl, J., Brenner, F. W. and Gheesling, L. L., 2001. Supplement 2000 (no. 44) to the Kauffmann–White scheme. Research in Microbiology 152, 907-909.

    Article  PubMed  CAS  Google Scholar 

  • Rane, S., 2011. Street vended food in developing world: hazard analyses. Indian Journal of Microbiology 51, 100-106.

    Article  PubMed  Google Scholar 

  • Ribot, E. M., Fair, M. A., Gautom, R., Cameron, D. N., Hunter, S. B., Swaminathan, B. and Barrett, T. J., 2006. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157 : H7 Salmonella and Shigella for PulseNet. Foodborne Pathogens and Disease 3, 59-67.

    Article  PubMed  CAS  Google Scholar 

  • Rigby, C. E., Pettit, J. R., Bentley, A. H., Spencer, J. L., Salomons, M. O. and Lior, H., 1982. The relationships of salmonellae from infected broiler flocks, transport crates or processing plants to contamination of eviscerated carcases. Canadian Journal of Comparative Medicine. Revue Canadienne de Medecine Comparee 46, 272-278.

    PubMed  CAS  Google Scholar 

  • Ruiz-de-Castaneda, R., Vela, A. I., Lobato, E., Briones, V. and Moreno, J., 2011. Prevalence of Salmonella and Yersinia in free-living pied flycatchers (Ficedula hypoleuga) in central Spain. Journal of Zoo and Wildlife Medicine 42, 313-316.

    Article  PubMed  Google Scholar 

  • Rusul, G., Khair, J., Radu, S., Cheah, C.T. and Yassin, R.M., 1996. Prevalence of Salmonella in broilers at retail outlets, processing plants and farms in Malaysia. International Journal of Food Microbiology 33, 183-194.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Vargas, F. M., Abu-El-Haija, M. A. and Gomez-Duarte, O. G., 2011. Salmonella infections: an update on epidemiology, management, and prevention. Travel Medicine and Infectious Disease 9, 263-277.

    Article  PubMed  Google Scholar 

  • Sarwari, A. R., Madger, L. S., Levine, P., Mc Namara, A. M., Knower, S., Armstrong, G. L., Etzel, R., Hollingsworth, J. and Morris, J. G., 2001. Serotype distribution of Salmonella isolates from food animals after slaughter differs from that of isolates found in humans. Journal of Infectious Diseases 183, 1295-1299.

    Article  PubMed  CAS  Google Scholar 

  • Sasipreeyajan, J., Jerngklinchan, J., Koowatananukul, C. and Saitanu, K., 1996. Prevalence of salmonellae in broiler, layer and breeder flocks in Thailand. Tropical Animal Health and Production 28, 174-180.

    PubMed  CAS  Google Scholar 

  • Shahada, F., Chuma, T., Okamoto, K. and Sueyoshi, M., 2008. Temporal distribution and genetic fingerprinting of Salmonella in broiler flocks from southern Japan. Poultry Science 87, 968-972.

    Article  PubMed  CAS  Google Scholar 

  • Sow, A. I., Seydi, M., Thiaw, M., Ndour, C. T., Soumare, C. T., Cisse, M. F., Badiane, S. and Samb, A., 2000. Les salmonelloses au centre hospitalier universitaire de Fann à Dakar : aspects bactériologiques. Médecine et Maladies Infectieuses 30, 657-660.

    Article  Google Scholar 

  • Switt, A. I. M., Soyer, Y., Warnick, L. D. and Wiedmann, M., 2009. Emergence, Distribution, and Molecular and Phenotypic Characteristics of Salmonella enterica Serotype 4,5,12:i. Foodborne Pathogens and Disease 6, 407-415.

    Article  PubMed  Google Scholar 

  • Tauxe, R., 1996. An Update on Salmonella. Health Environmental Digest 10, 1-4.

    Google Scholar 

  • Tenover, F. C., Arbeit, R. D., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H. and Swaminathan, B., 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. Journal of Clinical Microbiology 33, 2233-2239.

    PubMed  CAS  Google Scholar 

  • Thong, K. L., Goh, Y. L., Radu, S., Noorzaleha, S., Yasin, R., Koh, Y. T., Lim, V. K., Rusul, G. and Puthucheary, S. D., 2002. Genetic diversity of clinical and environmental strains of Salmonella enterica serotype Weltevreden isolated in Malaysia. Journal of Clinical Microbiology 40, 2498-2503.

    Article  PubMed  CAS  Google Scholar 

  • Threlfall, E. J., Graham, A., Cheasty, T., Ward, L. R. and Rowe, B., 1997. Resistance to ciprofloxacin in pathogenic Enterobacteriaceae in England and Wales in 1996. Journal of Clinical Pathology 50, 1027-1028.

    Article  PubMed  CAS  Google Scholar 

  • Trampel, D. W., Hasiak, R. J., Hoffman, L. J. and Debey, M. C., 2000. Recovery of Salmonella from water, equipment, and carcasses in turkey processing plants. Journal of Applied Poultry Research 9, 29-34.

    Google Scholar 

  • Tsai, H.J. and Hsiang, P.H., 2005. The prevalence and antimicrobial susceptibilities of Salmonella and Campylobacter in ducks in Taiwan. Journal of Veterinary Medical Science 67, 7-12.

    Article  PubMed  Google Scholar 

  • Usera, M. A., Aladuena, A., Gonzalez, R., De la Fuente, M., Garcia Pena, J., Frias, N. and Echeita, M. A., 2002. Antibiotic resistance of Salmonella spp. from animal sources in Spain in 1996 and 2000. Journal of Food Protection 65. http://research.bmn.com/medline/search/record?uid=MDLN.22025871, 768-773.

  • van_den_Bogaard, A. E. and Stobberingh, E. E., 2000. Epidemiology of resistance to antibiotics. Links between animals and humans. International Journal of Antimicrobial Agents 14. http://research.bmn.com/medline/search/record?uid=MDLN.20257109, 327-335.

  • Vo, A. T. T., Van Duijkeren, E., Fluit, A. C., Heck, M. E. O. C., Verbruggen, A., Maas, H. M. E. and Gaastra, W., 2006. Veterinary Microbiology 113, 153-158.

    Google Scholar 

  • W.H.O. 2002. GlobalSurv. http://www.who.int/foodsafety/foodborne_disease/surveillance/en/.

  • White, P. L., Baker, A. R. and James, W. O., 1997. Strategies to control Salmonella and Campylobacter in raw poultry products. Revue Scientifique et Technique (International Office of Epizootics) 16, 525-541.

    CAS  Google Scholar 

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Acknowledgments

We acknowledge the staff of Avi-pole Reunion for collaboration: Jef Reichardt, Jacky Berby, Jimmy Hoarau, François Penverne and Yvon Euzen; thanks to farmers for their participation. We acknowledge the staff of the slaughterhouse for the organization of the sample collection: François Gauvrit, Benjamin Boulanger and Guillaume Burel, Eric Pascal and his staff, Stephanie Yeung and Pierre Reype. We are grateful to the staff of the AFSSA HQPAP (Ploufragan) and AFSSA CEB laboratory to let us use their technical material.

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Correspondence to Isabelle Henry.

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An erratum to this article is available at http://dx.doi.org/10.1007/s11250-014-0555-z.

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Henry, I., Granier, S., Courtillon, C. et al. Salmonella enterica subsp. enterica isolated from chicken carcasses and environment at slaughter in Reunion Island: prevalence, genetic characterization and antibiotic susceptibility. Trop Anim Health Prod 45, 317–326 (2012). https://doi.org/10.1007/s11250-012-0221-2

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