Incidence and antimicrobial susceptibility of Salmonella, Listeria, and Campylobacter spp. in raw “souvlaki” marketed in Thessaloniki (Northern Greece)


Published: Jan 31, 2018
Keywords:
Salmonella Listeria Campylobacter souvlaki incidence antimicrobial susceptibility
N. SOULTOS (Ν. ΣΟΥΛΤΟΣ)
E. IOSSIFIDOU (Ε. ΙΩΣΗΦΙΔΟΥ)
E. PSOMAS (Ε. ΨΩΜΑΣ)
Z. TZIKAS (Ζ. ΤΖΗΚΑΣ)
T. LAZOU (Θ. ΛΑΖΟΥ)
Abstract

Souvlaki is a popular Greek meat product consisting of small chunks or cubes of pork threaded on a small wooden or metal skewer. In the present study, 105 samples of raw pork souvlaki obtained from retail shops in Thessaloniki (Northern Greece) were screened for the incidence of Salmonella, Listeria, and Campylobacter and their susceptibility to various antimicrobial agents; serotyping of the isolates was also performed. Of the samples tested, 1.9% were positive for Salmonella and yielded 3 serovars (S. SaintPaul, S. Fyris and S. Typhimurium); 31.4% proved positive for Listeria spp. with 6.7% yielding L. monocytogenes isolates belonged to molecular serogroups 2 (serotypes 1/2c and 3c) and 4 ( serotypes 4b, 4d, and 4e). Campylobacter spp. were not detected in any of the samples tested. The antimicrobial susceptibility to various antimicrobial agents of 11 Salmonella strains and 7 L. monocytogenes strains was also determined by disc diffusion method. Salmonella spp. were susceptible to a panel of 12 antibiotics but displayed intermediate resistance to tetracycline. L. monocytogenes isolates were resistant to nalidixic acid and ceftriaxone, partly resistant to clindamycin and cefotaxime, but sensitive to all antibiotics commonly used in veterinary and human listeriosis. Our findings indicate that souvlaki could be a potential vehicle of food borne infections due to strains of L. monocytogenes and Salmonella spp. in the case of inadequate thermal processing. In addition, good hygienic practices must be applied to avoid cross-contamination during preparation or handling of the product.

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References
Aslam M, Checkley S, Avery B, Chalmers G, Bohaychuk V, Genser G, Reid-Smith R, Boerlin P (2012) Phenotypic and genetic characterization of antimicrobial resistance in Salmonella serovars isolated from retail meats in Alberta, Canada. Food Microbiol 32:110-117.
Bauer AW, Kirby WMM, Sherris JC, Turk M (1966) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45:493-496.
Bohaychuk VM, Gensler GE, King RK, Manninen KI, Sorensen O, Wu JT, Stiles ME, Mc Mullen LM (2006) Occurrence of Pathogens in Raw and Ready-to-Eat Meat and Poultry Products Collected from the Retail Marketplace in Edmonton, Alberta, Canada. J Food Protect 69:2176-2182.
Boyen F, Haesebrouch F, Maes D, Van Immerseel F, Ducatelle R, Pasmans F (2008) Non typhoidal Salmonella infection in pigs: a closer look at epidemiology, pathogenesis and control. Vet Microbiol 130:1-9.
Busani L, Cigliano A, Taioli E, Caligiuri V, Chiavacci L, Di Bella C, Battisti A, Duranti A, Gianfranceschi M, Nardella MC, Ricci A, Rplesu S, Tamba M, Marabelli R, Caprioli A (2005) Prevalence of Salmonella enterica and Listeria monocytogenes Contamination in Foods of Animal Origin in Italy. J Food Protect 68:1729-1733.
Chen BY, Pyla R, Kim T-J, Silva JL, Jung Y-S (2010) Antibiotic resistance in Listeria species isolated in catfish fillets and processing environment. Lett Appl Microbiol 50:626-632.
Chen Y, Knabel SJ (2007) Multiplex PCR for simultaneous detection of the genus Listeria, Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes. Appl Environ Microbiol 73:6299-6304.
Charpentier E, Gerbaud G, Jacquet C, Rocourt J, Courvalin P (1995) Incidence of antibiotic resistance in Listeria species. J Infect Dis 172:277–281.
Cloak OM, Duffy G, Sheridan JJ, Blair IS, McDowell DA (2001) A survey on the incidence of Campylobacter spp. and the development of a surface adhesion polymerase chain reaction (SA-PCR) assay for the detection of Campylobacter jejuni in retail meat products. Food Microbiol 18:287-298.
Clinical and Laboratory Standards Institute (CLSI) (2008) Performance standards for antimicrobial susceptibility testing. Eighteenth Informational Supplement, CLSI document M100-S18. Wayne, PA.
Doumith M, Buchrieser C, Glaser P, Jacquet C Martin P (2004) Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 42:3819-3822.
Duffy EA, Belk KE, Sofos JN, Bellinger GR, Pape A, Smith GC (2001) Extent of microbial contamination in United States pork retail products. J Food Protect 64:172-178.
European Food Safety Authority (EFSA) (2014) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA Journal 12(2):3547.
Fosse J, Seegers H, Magras C (2008) Foodborne zoonoses due to meat: a quantitative approach for a comparative risk assessment applied to a pig slaughtering in Europe. Vet Res 39:01.
Ghafir Y, China B, Dierick K, De Zutter L, Daube G (2007) A seven year survey of Campylobacter contamination in meat at different production stages in Belgium. Int J Food Microbiol 116:111-120.
Giovannini A, Prencipe V, Conte A, Marino L, Petrini A, Pomilio F, Rizzi V, Migliorati G (2004) Quantitative risk assessment of Salmonella spp. infection for the consumer of pork products in an Italian region. Food Control 15:139-144.
Gomes-Neves E, Actunes P, Tavares A, Themudo P, Cardoso M F, Gärtner F, Costa JM, Peixe L (2012) Salmonella cross-contamination in swine abattoirs in Portugal: Carcasses, meat and meat handlers. Int J Food Microbiol 157:82-87.
Gray M, Zadoks RN, Fortes ED, Dogan B, Cai S, Chen Y, Scott VN, Gombas PE, Boor KJ (2004) Listeria monocytogenes isolates from foods and human from distinct but overlapping populations. Appl Environ Microb 70:5833-5841.
ISO 6579:2002 (2002) Microbiology of food and animal feed stuffs. Horizontal method for the detection of Salmonella species.
ISO 11290-1:1996/FDAM 1:2004(E) (2004) Microbiology of food and animal feeding stuffs – Horizontal method for detection and enumeration of L. monocytogenes - Part 1: Detection method. AMENDMENT 1: Modification of the isolation media and haemolysis test, and inclusion of precision data.
ISO 10272-1:2006(E) (2006) Microbiology of food and animal feeding stuffs – Horizontal method for detection and enumeration of Campylobacter spp. growing at 41,5ºC - Part 1: Detection method.
Jordan E, Egan J, Dullea C, Ward J, McGillicuddy K, Murray G, Murphy A, Bradshaw B, Leonard N, Rafter P, McDowell S (2006) Salmonella surveillance in raw and cooked meat products in the Republic of Ireland from 2002 to 2004. Int J Food Microbiol 112:66-70.
Karakolev R (2009) Incidence of Listeria monocytogenes in beef, pork, raw-dried and raw-smoked sausages in Bulgaria. Food Control 20:953-955.
Kathariou S (2002) Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J Food Protect 65:1811-1829.
Kérouanton A, Marault M, Petit L, Grout J, Dao TT, Brisabois A (2010) Evaluation of a multoplex PCR assay as an alternative method for Listeria monocytogenes serotyping. J Microbiol Meth 80:134-137.
Kornacki JL, Gurtler JB (2007) Incidence and control of Listeria in food processing facilities. In: (eds: Ryser ET, Marths EH) Listeria, listeriosis and food safety. Boca Raton, FL: CRC Press, pp. 681-766
Lawrence LM, Gilmour A (1994) Incidence of Listeria spp. and L. monocytogenes in a poultry processing environment and in poultry products and their rapid confirmation by multiplex PCR. Appl Environ Microbiol 60 (12):4600-4604.
Little CL, Richardson JF, Owen RJ, de Pinna E, Threfall EJ (2008) Campylobacter and Salmonella in raw meats in the United Kingdom: Prevalence, characterization and antimicrobial resis tance pattern, 2003-2005. Food Microbiol 25:538-543.
Liu D (2006) Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 55:645-659.
López Z, Vilatoro D, Ortiz S, López P, Navas J, Dávila JC, Martínez- Suárez JV (2008) Molecular tracking of Listeria monocytogenes in an Iberian pig abattoir and processing plant. Meat Sci 78(1-2):130-134.
Madden RH, Moran L, Scates P (1998) Frequency of occurrence of Campylobacter spp. in red meats and poultry in Northern Ireland and their subsequent subtyping using polymerase chain reaction-restriction fragment length polymorphism and the random amplified polymorphic DNA method. J Appl Microbiol 84:703-708.
Mataragas M, Skandamis PN, Drosinos EH (2008) Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. Int J Food Microbiol 126:1-12.
Mayrhofer S, Paulsen P, Smulders FJM, Hilbert F (2004) Antimicrobial resistance of five major food-borne pathogens isolated from beef, pork and poultry. Int J Food Microbiol 97:23-29.
O’Toole DK (1995) Technical Report: Microbiological quality of pork meat from local Hong Kong markets. World J Microb Biot 11:699-702.
Pesavento G, Ducci B, Nieri D, Comodo N, Lo Nostro A (2010) Prevalence and antibiotic susceptibility of Listeria spp. Isolated from raw meat and retail foods. Food Control 21:708-713.
Pezzotti G, Serafin A, Luzzi I, Mioni R, Milan M, Perin R (2003) Occurrence and resistance to antibiotics of Campylobacter jejuni and Campylobacter coli in animals and meat in northeastern Italy. Int J Food Microbiol 82:281-287.
Prendergast DM, Duggan SJ, Fanning S, Cormican M, Gonzales- Barron U, Butler F, Duffy G (2008) Prevalence and numbers of Salmonella spp. and Enterobacteriaceae on pork cuts in abattoirs in the Republic of Ireland. J Appl Microbiol 105:1209-1219.
Prendergast DM, Duggan SJ, Gonzales-Barron U, Fanning S, Butler F, Cormican M, Duffy G (2009) Prevalence, numbers and characteristics of Salmonella spp. on Irish retail pork. Int J Food Microbiol 131:233-239.
Schwaiger K, Hunter S, Hölzel C, Kämpf P, Bauer J (2012) Prevalence of antibiotic-resistant enterobacteriaceae isolated from chicken and pork meat purchased at the slaughterhouse and at retail in Bavaria. Germany. Int J Food Microbiol 154:206-211.
Sergelidis D, Abrahim A (2009) Adaptive response of Listeria monocytogenes to heat and its impact to food safety. Food Control 20(1):1-10.
Stern NJ, Green SS, Thaker N, Krout DJ, Chiou J (1984) Recovery of Campylobacter jejuni from fresh and frozen meat and poultry collected at slaughter. J Food Protect 47:372-374.
Stern NJ, Hernandez MP, Blankenship L, Deibel KE, Doores S, Doyle MP, Pierson HNgMD, Sofos JN, Sveum WH, Ewsthofgf DC (1985) Prevalence and distribution of Campylobacter jejuni and Campylobacter coli in retail meats. J Food Protect 48:595-599.
Swaminathan B, Cabane D, Zhang W, Cossart P (2007) L. monocytogenes. In: (eds: Doyle MP, Beuchat LR) Food Microbiology: Fundamentals and Frontiers. Washinhton, DC, USA: ASM Press, pp. 457-491.
Thai TH, Hirai T, Lan NT, Yamaguchi R (2012) Antibiotic resistance profiles of of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 156:147-155.
Thénevot D, Dernburg A, Vernozy-Rozand C (2006a) Listeria monocytogenes An updated review of in pork meat industry and its products. J Appl Microbiol 101:7-17.
Thénevot D, Delignette-Muller M-L, Christieans S, Leroy S, Kodjo A, Vernozy-Rozand C (2006b) Serological and molecular ecology of Listeria monocytogenes isolates collected from 13 French pork meat salting-curing plants and their products. Int J Food Microbiol 112:153-161.
Troxler R, von Graevenitz A, Funke G, Wiedemann B, Stock I (2000) Natural antibiotic susceptibility of Listeria species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri strains. Clin Microbiol Infect 6:525–535.
Tzikas Z, Eleftheriadou A, Soultos ND, Psomas E, Iossifidou E, Lazou T (2011) Microbiological condition of raw minced meat in Central Macedonia, Greece. Proceedings of the 3rd Pan-Hellenic Congress in Technology of Animal Production (Thessaloniki, Greece), pp. 353-362.
Valero A, Hernandez M, De Cesare A, Manfreda G, García_Gimero RM, González-García P, Rodríguez-Lázaro D (2014) Probabilistic approach for determining Salmonella spp. and L. monocytogenes concentration in pork meat from presence/absence microbiological data. Intl J Food Microbiol Article in press.
Wang XM, Lü XF, Yin L, Liu HF, Zhang WJ, Si W, Yu SW, Shao ML, Liu SG (2013) Occurrence and antimicrobial susceptibility of Listeria monocytogenes isolates from retail raw foods. Food Control 32:153-158.
Wesley IV, Larsen S, Scott Hurd H, McKean JD, Griffith R, Rivera F, Nannapaneni R, Cox M, Johnson M, Wagner D, de Martino M (2008) Low prevalence of Listeria monocytogenes in cull sows and pork. J Food Protect 71(3):545-549.
Whyte P, McGill K, Cowley D, Madden RH, Moran l, Scates P, Carrol C, O’Leary A, Fanning S, Collins JD, McNamara E, Moore JE, Cormican M (2004) Occurrence of Campylobacter in retail foods in Ireland. Int J Food Microbiol 95:111-118.
World Health Organisation (WHO) (2009) Critically important antimicrobials for human medicine. WHO advisory group on integrated surveillance of antimicrobial resistance (AGISAR). Copenhagen, 2nd revision, Available from: http://www.who.int/foodsafety/foodbornedisease/CIA _2nd_rev_2009.pdf. Accessed May 2011.
Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S, Shi L (2010) Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol 143:230-234.
Zanetti F, Varoli O, Stampi S, de Luca G (1996) Prevalence of thermophilic Campylobacter and Arcobacter butzleri in food of animal origin. Int J Food Microbiol 33:315-321.
Zhao C, Ge B, De Villena J, Sudler R, Yeh E, Zhao S, White DG, Wagner D, Meng J (2001) Prevalence of Campylobacter spp., Escherichia coli, and Salmonella Serovars in Retail Chicken,
Turkey, Pork, and Beef from the Greater Washington, D.C. Area. Appl Environ Microbiol 67(12):5431-5436.
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