Salmonella Enteritidis predominance determined by serotyping and real-time PCR in poultry-derived food and avian isolates

This study aimed to determine Salmonella enterica subspecies enterica serovar Enteritidis (SE) presence by conventional serotyping and SE-specific real-time PCR (SE-rPCR) in poultry-derived food and avian isolates in our laboratory Salmonella spp. collection. Conventional serotyping indicated that 32 (8 chicken meat, 10 egg, 14 avian) out of 56 (57%) isolates were SE, whereas 8 (3 chicken meat, 2 turkey meat, 3 avian) (14%) isolates were serogroup B, 6 (1 chicken meat, 1 egg, 4 avian) (11%) were serogroup C1, 4 (3 chicken meat, 1 turkey meat) (7%) were serogroup C2-C3, 4 (3 chicken meat, 1 turkey meat) (7%) were serogroup E4, and 2 (avian) (4%) isolates were categorized as nonserogrouped/nonserotyped. Thirty-three (8/18 chicken meat, 10/11 egg, 15/23 avian) out of 56 (59%) Salmonella isolates were positive by SE-rPCR. SE was determined as the most prevalent serotype in both of the tests regardless of the sample type. Conventional serotyping and SE-rPCR results were in agreement in all but 1 isolate. Considerably high relative accuracy (98%), sensitivity (100%), and specificity (96%) with almost perfect agreement between the two methods (Cohen's kappa = 0.96) indicated SE-rPCR as a reliable tool in the rapid identification of SE isolates to complement conventional serotyping.

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  • EFSA, ECDC. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 2014; 12: 3547.
  • European Council. Regulation (EC) No 2160/2003 of the European Parliament and of the Council and Regulation of 17 November 2003 on the Control of Salmonella and Other Specified Food-Borne Zoonotic Agents. OJ L 325, 12.12.2003. Brussels, Belgium: European Council; 2003.
  • European Council. Regulation on the Control of Salmonella and Other Specified Food-Borne Zoonotic Agents. Official Journal 27.03.2014; 28954. Brussels, Belgium: European Council; 2014.
  • Grimont PAD, Weill FX. Antigenic Formulae of the Salmonella Serovars. 9th ed. Paris, France: WHO Collaborating Centre for Reference and Research on Salmonella ; 2007.
  • Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PA, Weill FX. Supplement 2003-2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol 2010; 161: 26-29.
  • Wang SJ, Yeh DB, Wei CI. Specific PCR primers for the identification of Salmonella enterica serovar Enteritidis in chicken-related samples. J Food Drug Anal 2009; 3: 183-189.
  • Saeki EK, Alves J, Bonfante RC, Hirooka EY, De Oliveira TCRM. Multiplex PCR (mPCR) for the detection of Salmonella spp. and the differentiation of the Typhimurium and Enteritidis serovars in chicken meat. J Food Safety 2013; 33: 25-29.
  • Maurischat S, Baumann B, Martin A, Malorny B. Rapid detection and specific differentiation of Salmonella enterica subsp. enterica Enteritidis, Typhimurium and its monophasic variant 4,[5],12:i:- by real-time multiplex PCR. Int J Food Microbiol 2015; 193: 8-14.
  • Lungu B, Waltman WD, Berghaus RD, Hofacre CL. Comparison of a real-time PCR method with a culture method for the detection of Salmonella enterica serotype Enteritidis in naturally contaminated environmental samples from integrated poultry houses. J Food Prot 2012; 75: 743-747.
  • Coven F, Asiklar B, Coven N, Nalbantsoy A. Screening of Salmonella Enteritidis specific O and H antiserum potency against isolated field strains of Salmonella from Aegean region. Acta Sci Vet 2015; 43: 1272.
  • Kahya S, Kesin Tuğ B, Temelli S, Carli KT, Eyigor A. Detection of Salmonella from layer flocks and typing of the isolates. Kafkas Univ Vet Fak Derg 2014; 20: 939-944 (in Turkish with English abstract).
  • Dumen E, Aydin A, Issa G. Prevalence, serological typing and PCR sensitivity comparison of Salmonella Typhimurium, Salmonella Enteritidis and Salmonella spp. isolated from raw chicken carcasses. Kafkas Univ Vet Fak Derg 2015; 21: 653-658.
  • Temelli S, Eyigor A, Carli KT. Salmonella serogroup detection from poultry meat samples by examining multiple colonies from selective plates of two standard culture methods. Foodborne Pathog Dis 2010; 7: 1229-1234.
  • Temelli S, Kahya S, Ata Z, Carli KT, Eyigor A. Presence of Salmonella in retail grade a eggs determined by the International Organization for Standardization 6579 method and a LightCycler polymerase chain reaction system. Vet J Ankara Univ 2015; 62: 125-132.
  • Carli KT, Unal CB, Caner V, Eyigor A. Detection of Salmonellae in chicken feces by a combination of tetrathionate broth enrichment, capillary PCR, and capillary gel electrophoresis. J Clin Microbiol 2001; 39: 1871-1876.
  • ISO. Microbiology of Food and Animal Feeding Stuffs-Protocol for the Validation of Alternative Methods. ISO 16140:2003 (E). Geneva, Switzerland: International Organization for Standardization; 2003.
  • Kim MS, Lim TH, Jang JH, Lee DH, Kim BY, Kwon JH, Choi SW, Noh JY, Hong YH, Lee SB et al. Prevalence and antimicrobial resistance of Salmonella species isolated from chicken meats produced by different integrated broiler operations in Korea. Poultry Sci 2012; 91: 2370-2375.
  • Wang Y, Yang B, Wu Y, Zhang Z, Meng X, Xi M, Wang X, Xia X, Shi X, Wang D et al. Molecular characterization of Salmonella enterica serovar Enteritidis on retail raw poultry in six provinces and two National cities in China. Food Microbiol 2015; 46: 74-80.
  • Lai J, Wu C, Wu C, Qi J, Wang Y, Wang H, Liu Y, Shen J. Serotype distribution and antibiotic resistance of Salmonella in food-producing animals in Shandong province of China, 2009 and 2012. Int J Food Microbiol 2014; 180: 30-38.
  • Donado-Godoy P, Clavijo V, León M, Arevalo A, Castellanos R, Bernal J, Tafur MA, Ovalle MV, Alali WQ, Hume M et al. Counts, serovars, and antimicrobial resistance phenotypes of Salmonella on raw chicken meat at retail in Colombia. J Food Prot 2014; 77: 227-235.
  • Durul B, Acar S, Bulut E, Kyere EO, Soyer Y. Subtyping of Salmonella food isolates suggests the geographic clustering of serotype Telaviv. Foodborne Pathog Dis 2015; 12: 958-965.
  • Mainali C, Gensler G, McFall M, King R, Irwin R, Senthilselvan A. Evaluation of associations between feed withdrawal and other management factors with Salmonella contamination of broiler chickens at slaughter in Alberta. J Food Prot 2009; 72: 2202-2207.
  • Erol I, Goncuoglu M, Ayaz ND, Ellerbroek L, Bilir Ormanci FS, Kangal OI. Serotype distribution of Salmonella isolates from turkey ground meat and meat parts. Biomed Res Int 2013; 2013: 281591.
  • Folster JP, Campbell D, Grass J, Brown AC, Bicknese A, Tolar B, Joseph LA, Plumblee JR, Walker C, Fedorka-Cray PJ et al. Identification and characterization of multidrug-resistant Salmonella enterica serotype Albert isolates in the United States. Antimicrob Agents Chemother 2015; 59: 2774-2779.
  • Kinross P, van Alphen L, Martinez Urtaza J, Struelens M, Takkinen J, Coulombier D, Makela P, Bertrand S, Mattheus W, Schmid D et al. Multidisciplinary investigation of a multicountry outbreak of Salmonella Stanley infections associated with turkey meat in the European Union, August 2011 to January 2013. Euro Surveill 2014; 19: 20801.
  • Kottwitz LB, Leão JA, Back A, Rodrigues Ddos P, Magnani M, de Oliveira TC. Commercially laid eggs vs. discarded hatching eggs: contamination by Salmonella spp. Braz J Microbiol 2013; 44: 367-370.
  • Lublin A, Maler I, Mechani S, Pinto R, Sela-Saldinger S. Survival of Salmonella enterica serovar Infantis on and within stored table eggs. J Food Prot 2015; 78: 287-292.
  • Kinde H, Castellan DM, Kerr D, Campbell J, Breitmeyer R, Ardans A. Longitudinal monitoring of two commercial layer flocks and their environments for Salmonella enterica serovar Enteritidis and other Salmonellae. Avian Dis 2005; 49: 189-194.
  • Giombelli A, Gloria MB. Prevalence of Salmonella and Campylobacter on broiler chickens from farm to slaughter and efficiency of methods to remove visible fecal contamination. J Food Prot 2014; 77: 1851-1859.
  • Wattiau P, Boland C, Bertrand S. Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol 2011; 77: 7877-7885.
Turkish Journal of Veterinary and Animal Sciences-Cover
  • ISSN: 1300-0128
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK