ALİ GÜCÜKOĞLU, Özgür ÇADIRCI, Göknur TERZİ GÜLEL, TOLGA UYANIK, Sibel KANAT

Serotyping and Antibiotic Resistance Profile of Listeria monocytogenes Isolated from Organic Chicken Meat

In this study, 240 organic chicken pieces (80 thighs, 80 wings, 80 skinless-breast meat) were analyzed for the presence of Listeria monocytogenes. Within the framework of the analysis findings; L. monocytogenes was detected in 60 (25%) of all 240 collected samples. In particular, L. monocytogenes was detected in 24 (30%) of 80 thigh samples, 20 (25%) of 80 wing samples and 16 (20%) of 80 skinless-breast meat samples. Serotyping distribution of 96 L. monocytogenes isolates determined as 71.8% serotype 1/2a, 21.9% serotype 1/2b, 4.2% serotype 4b and 2.1% serotype 1/2c. According to antibiotic resistance profile, 26 isolates (27%) were found to be resistant to ampicillin. The other isolates were found to be resistant to meropenem, tetracycline, sulfamethoxazole/trimethoprim, penicillin G, amoxicillin/clavulanic acid, vancomycin, oxytetracycline, erythromycin and chloramphenicol as 23 (23.9%), 14 (14.5%), 13 (13.5%), 12 (12.5%), 9 (9.3%), 7 (7.2%), 5 (5.2%), 4 (4.1%) and 3 (3.1%) respectively. Multiple antibiotic resistance profiles were determined in 12 of L. monocytogenes isolates. The findings of this study are thought to be unique data for serotyping studies that will help in revealing the epidemiology of L. monocytogenes in organic poultry meat, enterprises operating in food sector and diagnosis and treatment of listeriosis.

Organik Tavuk Etlerinden İzole Edilen Listeria monocytogenes İzolatlarının Serotip ve Antibiyotik Direnç Profilinin Belirlenmesi

Bu çalışmada, 240 organik tavuk parça eti (80 but, 80 kanat, 80 derisiz-göğüs eti) Listeria monocytogenes varlığı yönünden analiz edildi. Analiz bulguları çerçevesinde; toplam 240 örneğin 60’ında (%25) L. monocytogenes saptandı. Bulgularının örneklere göre dağılımı incelendiğinde; but örneklerinin 24’ünde (24/80-%30), kanat örneklerinin 20’sında (20/80-%25), derisiz göğüs eti örneklerinin ise 16’sında (16/80-%20) L. monocytogenes tespit edildi. Serotip dağılımında ise but örneklerinden elde edilen 40 L. monocytogenes izolatının 31’inin L. monocytogenes 1/2a, 6’sının L. monocytogenes 1/2b, 3’ünün L. monocytogenes 1/2c, 1’inin ise L. monocytogenes 4b serotipinde olduğu, kanat örneklerinden elde edilen 34 L. monocytogenes izolatının 24’ünün L. monocytogenes 1/2a, 9’unun L. monocytogenes 1/2b, 1’inin ise L. monocytogenes 4b serotipi olduğu, derisiz göğüs eti örneklerinden elde edilen 22 L. monocytogenes izolatının 14’ünün L. monocytogenes 1/2a, 6’sının L. monocytogenes 1/2b, 2’sinin ise L. monocytogenes 4b serotipi olduğu belirlendi. Antibiyotik direnç profiline bakıldığında; 26 izolat (%27) ampisiline dirençli bulunurken, meropenem, tetrasiklin, sülfametoksazol/trimetoprim, penisilin G, amoksisilin/klavulanik asit, vankomisin, oksitetrasiklin, eritromisin ve kloramfenikole karşı dirençli izolat sayısı sırası ile 23 (%23.9), 14 (%14.5), 13 (%13.5), 12 (%12.5), 9 (%9.3), 7 (%7.2), 5 (%5.2), 4 (%4.1) ve 3 (%3.1) olarak saptandı. L. monocytogenes izolatlarının 12’sinde ise çoklu antibiyotik direnç profili belirlendi. Sonuç olarak bu çalışmada tespit edilen bulguların L. monocytogenes’in organik kanatlı etlerinde epidemiyolojisini ortaya koyacak serotiplendirme çalışmalarına, gıda sektöründe faaliyet gösteren işletmelere ve listeriyosizin tanı ve tedavisinde özgün veri niteliğinde olacağı düşünülmektedir.

___

1. Fanatico AC, Pillai PB, Emmert JL, Owens CM: Meat quality of slow and fast growing chicken genotypes fed low nutrient or standard diets and raised indoors or with outdoor access. Poult Sci, 86, 2245-2255, 2007. DOI: 10.1093/ps/86.10.2245

2. Alali WQ, Thakur S, Berghaus RD, Martin MP, Gebreyes WA: Prevalence and distribution of salmonella in organic and conventional broiler poultry farms. Foodborne Pathog Dis, 7, 1363-1371, 2010. DOI: 10.1089/fpd.2010.0566

3. Food and Agriculture Organization of the United Nations (FAO): Organic agriculture and the law, 2012.

4. Rouger A, Tresse O, Zagorec M: Bacterial contaminants of poultry meat: Sources, species, and dynamics. Microorganisms, 5:50, 2017. DOI: 10.3390/microorganisms5030050

5. Miranda JM, Vazquez BI, Fente CA, Calo-Mata P, Cepeda A, Franco CM: Comparison of antimicrobial resistance in Escherichia coli, Staphylococcus aureus and Listeria monocytogenes strains isolated from organic and conventional poultry meat. J Food Prot, 71, 2537-2542, 2008. DOI: 10.4315/0362-028x-71.12.2537

6. Cui S, Ge B, Zheng J, Meng J: Prevalence and antimicrobial resistance of Campylobacter spp. and Salmonella serovars in organic chickens from Maryland retail stores. Appl Environ Microbiol, 71 (7): 4108-4111, 2005. DOI: 10.1128/AEM.71.7.4108-4111.2005

7. Rosenquist H, Boysen L, Krogh AL, Jensen AN, Nauta M: Campylobacter contamination and the relative risk of illness from organic broiler meat in comparison with conventional broiler meat. Int J Food Microbiol, 162 (3): 226-230, 2013. DOI: 10.1016/j.ijfoodmicro.2013.01.022

8. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control): The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J, 14:4634, 2016

9. Buchanan RL, Gorris LGM, Hayman MM, Jackson TC, Whiting RC: A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control, 75, 1-13, 2017. DOI: 10.1016/j.foodcont.2016.12.016

10. Jamshidi A, Zeinali T: Significance and characteristics of Listeria monocytogenes in poultry products. Int J Food Sci, 2019:7835253, 2019. DOI: 10.1155/2019/7835253

11. ISO 11290-1: Microbiology of the Food Chain -Horizontal Method for the Detection and Enumeration of Listeria monocytogenes and of Listeria spp. Part 1: Detection Method. 2017.

12. Dynal AS: Cell Separation and Protein Purification, Technical Handbook. 2nd ed., Dynal AS. Norway Printed. 02 96, 1996.

13. Bohnert M, Dilasser F, Dalet C, Mengaud J, Cossart P: Use of specific oligonucleotides for direct enumeration of Listeria monocytogenes in food samples by colony hybridization and rapid detection by PCR. Res Microbiol, 143, 271-280, 1992. DOI: 10.1016/0923-2508(92)90019-k

14. Doumith M, Buchrieser C, Glaser P, Jacquet C, Martin P: Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol, 42 (8): 3819-3822, 2004. DOI: 10.1128/JCM.42.8.3819-3822.2004

15. Clinical and Laboratory Standards Institute (CLSI): Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria. 3rd ed, CLSI Guideline M45. Wayne, PA; 2016.

16. The European Committee on Antimicrobial Susceptibility Testing (EUCAST): Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 7.1, 2017.

17. Schafer DF, Steffens J, Barbosa J, Zeni J, Paroul N, Valduga E, Junges A, Backes GT, Cansian RL: Monitoring of contamination sources of Listeria monocytogenes in a poultry slaughterhouse. LWT- Food Sci Technol, 86, 393-398, 2017. DOI: 10.1016/j.lwt.2017.08.024

18. Rahmat GR, Ibrahim A, Bakar FA: Prevalence of Listeria monocytogenes in retail beef and poultry. Pertanika, 14 (3): 249-255, 1991.

19. Weis J: Vorkommen von Listerien in Hackfleisch. Tierarztl Umsch, 52 (7): 456-458, 1989.

20. Farber JM, Sanders GW, Johnston MA: A survey of various foods for the presence of Listeria species. J Food Prot, 52 (7): 456-458, 1989. DOI: 10.4315/0362-028X-52.7.456

21. Elmalı M, Can HY, Yaman H: Prevalence of Listeria monocytogenes in poultry meat. Food Sci Technol, 35 (4): 672-675, 2015. DOI: 10.1590/1678457X.6808

22. Bailey JS, Fletcher DL, Cox NA: Recovery and serotype distribution of L. monocytogenes from broiler chickens in southeastern United States. J Food Prot, 52 (3): 148-150, 1989. DOI: 10.4315/0362-028X-52.3.148

23. Rorvik LM, Aase B, Alvestad T, Caugant DA: Molecular epidemiological survey of Listeria monocytogenes in broilers and poultry products. J Appl Microbiol, 94, 633-640, 2003. DOI: 10.1046/j.1365-2672.2003.01895.x

24. Alsheikh ADI, Mohammed GE, Abdalla MA: Isolation and identification of Listeria monocytogenes from retail broiler chicken ready to eat meat products in Sudan. Int J Anim Vet Adv, 5 (1): 9-14, 2013. DOI: 10.19026/ijava.5.5570

25. Alsheikh ADI, Mohammed GE, Abdalla MA, Bakhiet AO: First isolation and identification of Listeria monocytogenes isolated from frozen and shock frozen dressed broiler chicken in Sudan. Br Microbiol Res J, 4 (1): 28-38, 2014. DOI: 10.9734/BMRJ/2014/2449

26. Genigeorgis CA, Dutulescu D, Garayzabal JF: Prevalence of Listeria spp. in poultry meat at supermarket and slaughterhouse level. J Food Prot, 52 (9): 618-624, 1989.

27. Zeinali T, Jamshidi A, Bassami M, Rad M: Isolation and identification of Listeria spp. in chicken carcasses marketed in northeast of Iran. Int Food Res J, 24 (2): 881-887, 2017.

28. Basaran Kahraman B, Issa G, Kahraman T: Prevalence, antimicrobial resistance and molecular characterization of Salmonella spp. and Listeria monocytogenes isolated from chicken carcass. Kafkas Univ Vet Fak Derg, 24 (5): 775-779, 2018. DOI: 10.9775/kvfd.2018.19754

29. Carvalho FT, Vieira BS, Vallim DC, Carvalho LA, Carvalho RCT, Pereira RCL, Figueiredo EES: Genetic similarity, antibiotic resistance and disinfectant susceptibility of Listeria monocytogenes isolated from chicken meat and chicken-meat processing environment in Mato Grosso, Brazil. LWT- Food Sci Technol, 109, 77-82. 2019. DOI: 10.1016/j.lwt.2019.03.099

30. Oliveira TS, Varjão LM, da Silva LNN, Pereira, RCL, Hofer E, Vallim DC, Almeida RCC: Listeria monocytogenes at chicken slaughterhouse: Occurrence, genetic relationship among isolates and evaluation of antimicrobial susceptibility. Food Control, 88, 131-138, 2018. DOI: 10.1016/ j.foodcont.2018.01.015

31. Zeinali T, Jamshidi A, Bassami M, Rad M: Serogroup identification and virulence gene characterization of Listeria monocytogenes isolated from chicken carcasses. Iranian J Vet Sci Technol, 7 (2): 9-19, 2015. DOI: 10.22067/veterinary.v7i2.43658

32. Arslan S, Baytur S: Prevalence and antimicrobial resistance of Listeria species and subtyping and virulence factors of Listeria monocytogenes from retail meat. J Food Saf, 39:e12578, 2019. DOI: 10.1111/jfs.12578

33. Zeinali T, Jamshidi A, Rad M, Bassami M: A comparison analysis of Listeria monocytogenes isolates recovered from chicken carcasses and human by using RAPD PCR. Int J Clin Exp Med, 8 (6): 10152-10157, 2015.

34. Maung AT, Mohammadi TN, Nakashima S, Liu P, Masuda Y, Honjoh K, Miyamoto T: Antimicrobial resistance profiles of Listeria monocytogenes isolated from chicken meat in Fukuoka, Japan. Int J Food Microbiol, 304, 49-57, 2019. DOI: 10.1016/j.ijfoodmicro.2019.05.016

35. Erol I, Ayaz ND: Serotype distribution of Listeria monocytogenes isolated from turkey meat by multiplex PCR in Turkey. J Food Saf, 31, 149153, 2011. DOI: 10.1111/j.1745-4565.2010.00278.x

36. Walsh D, Duffy G, Sheridan JJ, Blair IS, McDowell DA: Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods. J Appl Microbiol, 90, 517-522, 2001. DOI: 10.1046/j.1365-2672. 2001.01273.x

37. Davis JA, Jackson CR: Comparative antimicrobial susceptibility of Listeria monocytogenes, L. innocua and L. welshimeri. Microb Drug Resist, 15, 27-32, 2009. DOI: 10.1089/mdr.2009.0863

38. Harakeh S, Saleh I, Zouhairi O, Baydoun E, Barbour E, Alwan N: Antimicrobial resistance of Listeria monocytogenes isolated from dairy based products. Sci Total Environ, 407, 4022-4027, 2009. DOI: 10.1016/j. scitotenv.2009.04.010

39. Rahimi E, Ameri M, Momtaz H: Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran. Food Control, 21, 1448-1452, 2010. DOI: 10.1016/j.foodcont.2010.03.014

40. Bilir Ormancı FS, Erol I, Ayaz ND, Iseri O, Sariguzel D: Immunomagnetic seperation and PCR detection of Listeria monocytogenes in turkey meat and antibiotic resistance of the isolates. Br Poult Sci, 49 (5): 560-565, 2008. DOI: 10.1080/00071660802298328

41. Lemes-Marques EG, Cruz CD, Destro MT: Pheno and ghenotypic characterization of Listeria monocytogenes clinical isolates from the south-western region of the state of Sao-Paolo, Brazil. Braz J Microbiol, 38, 287-292, 2007. DOI: 10.1590/s1517-83822007000200019

42. Filiousis G, Johansson A, Frey J, Perreten V: Prevalance, genetic diversity and antimicrobial susceptibility of Listeria monocytogenes isolated from open-air food markets in Greece. Food Control, 20, 314-317, 2009. DOI: 10.1016/j.foodcont.2008.05.018

43. Osaili TM, Alaboudi AR, Nesiar EA: Prevalence of Listeria spp. and antibiotic susceptibility of Listeria monocytogenes isolated from raw chicken and ready-to-eat chicken products in Jordan. Food Control, 22, 586-590, 2011. DOI: 10.1016/j.foodcont.2010.10.008

44. Conter M, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri V: Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int J Food Microbiol, 128, 497-500, 2009. DOI: 10.1016/j. ijfoodmicro.2008.10.018

45. Yan H, Neogi SB, Mo Z, Guan W, Shen Z, Zhang S, Li L, Yamasaki S, Shi L, Zhong N: Prevalence and characterization of antimicrobial resistance of foodborne Listeria monocytogenes isolates in Hebei province of Northern China, 2005-2007. Int J Food Microbiol, 144, 310-316, 2010. DOI: 10.1016/j.ijfoodmicro.2010.10.015

46. Okada Y, Okutani A, Suzuki H, Asakura H, Monden S, Nakama A, Maruyama T, Igimi S: Antimicrobial susceptibilities of Listeria monocytogenes isolated in Japan. J Vet Med Sci, 73 (12): 1681-1684, 2011. DOI: 10.1292/jvms.11-0051

47. Biavasco F, Giovanetti E, Miele A, Vignaroli C, Facinelli B, Varaldo PE: In vitro conjugative transfer of VanA vancomycin resistance between Enterococci and Listeria of different species. Eur J Clin Microbiol Infect Dis, 15, 50-59, 1996. DOI: 10.1007/bf01586185

48. Charpentier E, Courvalin P: Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother, 43 (9): 2103-2108, 1999.