Isolation of Salmonella spp. and Listeria monocytogenes from Chicken Internal Organs Retailed in Afyonkarahisar by Immonomagnetic Seperation Method and Determination of Antibiotic Resistance of Isolates

Öz

This study consists of 100 hearts and gizzards offered for retailed in Afyonkarahisar between August 2013 and February 2015. It was aimed to determine L. monocytogenes and Salmonella species by immunomagnetic separation technique in a total of 300 chicken internal organs and to determine the antibiotic susceptibility profiles of the isolates. 13% (39/300) Salmonella spp. 2.6% L. monocytogenes were detected in internal organ samples. The 39 Salmonella spp. 9 of the isolates were isolated from the heart (23.2%), 1 from the gizzard (2.5%), 29 (74.3%) from the liver. According to the internal organ type of L. monocytogenes isolate numbers are; 2 (25%) from the heart, 5 (62.5%) from the stone, and 1 (12.5%) from the liver. Salmonella spp. 100% of its isolates are tetracycline, chlortetracycline, and oxytetracycline, 64.1% to penicillin, 48.7% to ampicillin, 46.1% to florphenicol, 43.5% to amoxicillin resistance was found to be 26% to streptomycin, 15.3% to enrofloxacin and 7.6% to trimethoprim/sulfadiazine, whereas resistance to gentamicin was observed. 62.5% of isolates to tetracycline, chlortetracycline, oxytetracycline and trimethoprim / sulfadiazine, 50% to amoxicillin, florphenicol, 37.5% to enrofloxacin, 25% to ampicillin and penicillin 12.5% were found to be resistant to streptomycin. Gentamicin resistance was not detected in any of the Salmonella spp. and L. monocytogenes isolates.

Anahtar Kelimeler

• Antibiotic resistance
• Internal organ
• Salmonella spp.
• L. monocytogenes

Afyonkarahisar’da Satışa Sunulan Tavuk İç Organlarından Salmonella spp. ve Listeria monocytogenes’in İmmonomagnetik Seperasyon Yöntemi ile İzolasyonu ve İzolatların Antibiyotik Dirençliliğinin Belirlenmesi

Öz

Bu çalışmada, Ağustos 2013-Şubat 2015 tarihleri arasında Afyonkarahisar’da tüketime sunulan 100’er adet yürek, taşlık ve ciğerden oluşan toplam 300 tavuk iç organ örneğinde, L. monocytogenes ve Salmonella türlerinin immunomagnetik seperasyon tekniği ile saptanması, izolatların antibiyotik duyarlılık profillerinin belirlenmesi amaçlanmıştır. İç organ örneklerinden %13 Salmonella spp. ve %2,6 L. monocytogenes saptandı. Elde edilen 39 Salmonella spp. izolatının 9’u yürekten (%23,2), 1’i taşlıktan (%2,5), 29’u (%74,3) karaciğerden izole edildi. L. monocytogenes’in iç organ çeşidine göre izolat sayıları sırasıyla; yürekten 2 (%25), taşıktan 5 (%62,5) ve karaciğerden 1 (%12,5) adet olarak belirlendi. Salmonella spp. izolatlarının %100’ünün tetrasiklin, klortetrasiklin ve oksitetrasiklin’e, %64,1’inin penisilin’e, %48,7’si ampisilin’e, %46,1’inin florfenikol’e, %43,5’inin amoksisilin’e, %26’sının streptomisin’e, %15,3’ünün enrofloksasin’e, %7,6’sının trimetoprim/sülfadiazin’e dirençli olduğu saptanırken, gentamisin dirençliliği gözlendi. Elde edilen L. monocytogenes izolatlarının %62,5’inin tetrasiklin, klortetrasiklin, oksitetrasiklin ve trimetoprim/sülfadiazin’e, %50’sinin amoksisilin’e, florfenikol’e, %37,5’inin enrofloksasin’e, %25’inin ampisilin ve penisilin’e, %12,5’inin streptomisin’e dirençli olduğu belirlendi. Salmonella spp. ve L. monocytogenes izolatlarının hiçbirinde gentamisin direnci saptanmadı. Salmonella spp. ve L. monocytogenes izolatlarının en az bir ve daha fazla antibiyotiğe çoklu dirençli oldukları belirlendi.

Anahtar Kelimeler

• İç organ
• Antibiyotik direnci
• IMS
• Salmonella spp.
• L.monocytogenes

Kaynakça

1. Abd-Elghany SM., Sallam KI, Abd-Elkhalek A, Tamura T. Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol Infect. 2015; 143(5): 997-1003.
2. Abdellah C, Fouzıa RF, Abdelkader C, Rachida SB, Mouloud Z. Occurence of Salmonella in chicken carcasses and giblets in Meknes-Morocco. Pakistan J Nutri. 2008; 7(2): 231-233.
3. Abdellah C, Fouzia, RF, Abdelkader C, Rachida SB, Mouloud Z. Prevalance and anti-microbial susceptibility of Salmonella isolates from chicken carcasses and giblets in Meknes, Morocco. African J Mic Res. 2009; 3(5): 215-219.
4. Allerberger F, Wagner M. Listeriosis: a resurgent foodborne infection. Clin Microbiol Infect. 2010; 16(1): 16-23.
5. Alonso-Hernando A, Prieto M, Garcia-Fernandez C, Alonso-Calleja C, Capita R. Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control. 2012; 23: 37-41.
6. Andersson D, Balaban N, Baquero F, Courvalin, P, Glaser P. Antibiotic resistance: turning evolutionary principles into clinical reality, FEMS Microbiol Rev. 2020; 44(2): 171-188. Anonymous. http://fka.gov.tr; Erişim tarihi: 15.09.2018. Kanatlı hayvancılık sektör raporu. 2016.
7. Anonymous. 2017. Türk Gıda Kodeksi Hayvansal Gıdalarda Bulunabilecek Farmakolojik Aktif Maddelerin Sınıflandırılması ve Maksimum Kalıntı Limitleri Yönetmeliği, Resmi Gazete, 7 Mart, 2017, Sayı 3000.
8. Arroyo G, Arroyo JA. Detection of Salmonella serotypes in edible organ meats from markets in Madrid, Spain. Food Microbiol. 1995a; 12: 13-20.

9. Arroyo G, Arroyo JA. Efficiency of different enrichment and isolation procedures for the detection of Salmonella serotypes in edible offal. Journal of Applied Bacteriology, 1995b; 79(4): 360-367.
10. Arumugaswamy RK, Rahamat Ali GR, Abd Hamid SN. Prevalence of Listeria monocytogenes in foods in Malaysia. Int J Food Microbiol. 1994; 23(1): 117-121.
11. Awaisheh SS. Survey of Listeria monocytogenesand other Listeria spp.,contamination in different common ready-to-eat food products in Jordan. Pakistan J Biol Sci. 2009; 12(23): 1491-1497.
12. BAM. Bacteriological Analytical Manual, Food and Drug Administration Salmonella, 8 th Ed., AOAC International, USA. 2015.
13. BAM Bacteriological Analytical Manual, Food and Drug Administration, Detection and Enumeration of Listeria monocytogenes in foods, Chapter, 10. 2016.
14. Besd Bir. http://www.besdbir.org (Erişim Tarihi: 15.09.2018). Beyaz et sanayicileri ve damızlıkçıları birliği derneği, 2016.
15. Berche P. Pathophysiology and epidemiology of listeriosis. Bull L'Acad Nati Med. 2005; 189(3):507-16.
16. Brizioa P, Antheroa G. Moela de frango: Estudo da Prevalencia de Salmonella spp. Rev Brasil Pesquisa Alimentos. 2013; 4(2): 66-68. Broome J. Fairness proceedings of the Aristotelian Society. 1990; 91: 87-101.
17. Bonny, AC, Karou GT, Francine Ake MD, Dadie AT, Bohoua LG, Niamké SL. Distribution of serovars and antibiotic resistance genes of Salmonella isolated from chicken gizzards in Abidjan, Côte d’Ivoire International J Innov App Studies, 2015; 11(3): 567-578.
18. Capita R, Calleja CA, Prieto M. Prevalence of Salmonella enterica serovars and genovars from chicken carcasses in slaughterhouses in Spain. J App Microbiol. 2007; 103:1366-1375.
19. Cohen E, Davidovich M, Rokney A, Valinsky L, Rahav G, Mor O. Emergence of new variants of antibiotic resistance genomic islands among multidrug‐resistant Salmonella enterica in poultry. Environ Microbiol. 2020; 22 (1): 413-432.
20. Conter M, Paludi D, Zanardi E, Ghidinis, Vergara A, Ianieri A. Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int J Microbiol. 2009; 128: 497-500.
21. Cornell J, Neal KR. Protracted outbreak of Salmonella Typhimurium definitive phage type 170 food poisining related to tripe, ‘pig bag’, and chitterlings. Commun Dis Public Health. 1998; 1: 28-30.
22. Çolak NB, Hampikyan H. İstanbul piyasasında satışa sunulan sakatatlarda bazı anabolizan kalıntılarının mevcudiyeti üzerine bir çalışma. İstanbul Üniv Vet Fak Derg. 2005; 31 (1): 83-92.
23. Dhanashree B, Otta SK, Karunasagar I, Goebel W, Karunasagar I. Incidence of Listeria spp. in clinical and food samples in Mangalore, India. Food Microbiol. 2003; 20: 447-453.
24. Diane G, Newell A, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, Van Der Giessen J, Kruse H. Food-borne diseases. The challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol. 2010; 139: 3-15.
25. Dong P, Zhu L, Mao Y, Liang R, Niu L, Zhang Y. Prevalence and profile of Salmonella from samples along the production line in Chinese beef processing plants. Food Control. 2014; 38: 54-60.
26. Donoghue DJ. Antibiotic Residues In Poultry Tissues and Eggs: Human Health Concerns? Poultry Sci. 2003; 82: 618-621.
27. EFSA. http://www.europa.eu/en/efsajournal/doc/271r.pdf. (Erişim Tarihi: Ağustos, 2014). European Food Safety Authority The community summary report on food-borne outbreaks in the European Union in 2007; 2009
28. FAO. http://www.fao.org. 2013. (Erişim Tarihi: 15.05.2013) Food And Agrıculture Organızatıon of The United Nations.
29. FAOSTAT FAO. http://faostat3.fao.org/home/index.html≠SEARCH_DATA. 2018. (Erişim tarihi: 22 Haziran 2013). Food and Agriculture Organization. Offals.
30. Fernández EA, Calleja,AC, Fernández GC, Capıta R. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: Comparison between 1993 and 2006. Int J Food Microbiol. 2012; 153: 281-287.
31. Glasgow L, Forde M, Bro, D, Mahone YC, Fletcher S. Antibiotic use in poultry production in Grenada. Vet Med Int. 2019; 1-7.
32. Göncüoğlu M, Ormancı FSB, Uludağ M, Çil GI. Prevalence and Antibiotic Resistance of Salmonella spp. and Salmonella Typhimurium in Broiler Carcasses Wings and Liver. J Food Saf. 2016; 36(4): 524-31.
33. Guran H, Çiftçi R, Gürsoy N, Özekinci T, Alalı W. Prevalence of antibiotic-resistant Salmonella in retail organic chicken. British Food J. 2020; 1238-1251.
34. Hernando AA, Prieto M, Fernandez CG, Calleja CA, Capıta R. Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control. 2012; 23: 37-41.
35. Hur J, Kim JH, Park JH, Lee YJ, Lee JH. Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strain isolated from poultry. The Vet J. 2010; 189: 306-311.
36. Huis In’t Veld JHJ, Mulder RWAW, Snijders JMA. Impact of animal husbandry and slaughter technologies on microbial contamination of Meat: Monitoring and Control, Meat Science. 1994; 36: 123-154.
37. Inoue S, Nakama A, Ara Y, Kokubo Y, Maruyama T, Saito A, Yoshida T, Terao M, Yamamoto S, Kumagai S. Short communication: prevalence and contamination levels of Listeria monocytogenes in retail foods in Japan. Int J Food Microb. 2000; 59: 73-77.
38. Jamsiıdi A, Zeinali. Significance and characteristics of Listeria monocytogenes in poultry products. Int J Food Sci. 2019; 1-7.
39. Jung Y, Porto Fett A, Shoyer B, Luchansky J. Prevalence, levels, and viability of Salmonella in and on raw chicken livers, J Food Prot. 2019; 82 (5): 834-843.
40. Karou GT, Bonny AC, Ouattara GH, Dadie AT, Ahonzonıamke SL. Prevalence of Salmonella and microbial resistance of serovars in retail chicken gizzards. Int J Med App Sci. 2013a; 2 (4): 223-233.
41. Karou GT, Quattara H, Bakayoko S. Prevalence of Salmonella and distribution of serovars ısolated from retail raw chicken gizzard in Abidjan, Cote D’ivoire. Octa J Biosci. 2013b; 1(2): 115-121.
42. Kılınç Ü, Aydın F. Kayseri yöresindeki tavukçuluk işletmelerinden toplanan tavuklardan izole edilen salmonella türlerinin antibiyotiklere duyarlılıkları. Sağ Bil Derg. 2006; 15(1) 35-40.
43. Kuan CH, Wong WC, Pui CF, Mahyudin NA, Tang JYH, Nishibuchi, M, Radu S. Prevalence and quantification of Listeria monocytogenes in beef offal at retail level in Selangor, Malaysia.Brazil J Microbiol. 2013a; 44(4): 1169-1172.
44. Kuan CH, Goh, SG, Loo YY, Chang WS, Lye YL, Puspanadan S, Tang JYH, Nakaguchi Y, Nishibuchi M, Mahyudin NA, Radu S. Prevalence and quantification of Listeria monocytogenes in chicken offal at the retail level in Malaysia. Poultry Sci. 2013b; 92: 1664-1669.
45. Mena C, Almeida G, Carneiro L, Teixeira P, Hogg T, Gibbs PA. Incidence of Listeria monocytogenes in different food products commercialized in Portugal, Food Microbiol. 2004; 21: 213-216.
46. Miranda JM, Mondragón AC, Martinez, B, Guarddon M, Rodriguez JA. Prevalence and antimicrobial resistance patterns of Salmonella from different raw foods in Mexico. J Food Protec. 2009; 5: 926-1138.
47. Molla B, Mesfın A. A survey of Salmonella contamination in chicken carcass and giblets in Central Ethiopia. Revue Med Vet. 2003; 154(4): 267-270.
48. Molla B, Mesfın A, Alemayehu D. Multiple antimicrobial-resistant Salmonella serotypes isolated from chicken carcass and giblets in Debre Zeit and Addis Ababa, Ethiopia. Ethiop J Health Dev. (2003a); 17(2): 131-149.
49. NCCLS. Performance standards for antimicrobial disk susceptibility tests, 8 th Ed., Pennsylvannia, USA. 2003.
50. Nollet LML, Toldra F. Handbook of Analysis of Edible Animal By-Products. CRC Press, Taylor and Francis Group, NW, USA. 2011.
51. Odumeru JA, León-Velarde CG. Salmonella detection methods for food and food ingredients, In: Salmonella- a dangerous foodborne pathogen, Ed; Barakat Mahmoud SM, Rijeka JT, Croatia. 2012; pp. 373-392. Okorie-Kanu J, Madubuike A, Ezenduka E, Mgbeahuruike A. Occurrence and antibiogram of Listeria species in raw pork, beef, and chicken meats marketed in Enugu State, Southeast Nigeria, Vet World. 2010; 13(2): 317-325.
52. Oliver J, Gooch C, Lansing S, Schueler J, Hurst J. Fate of antibiotic residues, antibiotic-resistant bacteria, and antibiotic resistance genes in US dairy manure management systems. J Dairy Sci. 2020; 103(2): 1051-1071.
53. Oral AI Tavuk iç organlarında Salmonella Enteritidis’in izolasyonu ve izole edilen suşların antibiyotiklere duyarlılıklarının belirlenmesi. Adnan Menderes Üniv Sağ Bil Enst, Yüksek Lisans Tezi. 2008.
54. Pan ZM, Geng SZ, Ahou YQ, Liu ZY, Fang Q, Liu BB, JIao XA. Prevalence and antimicrobial resistance of Salmonella spp., isolated from domestic animals in eastern China. J Animal Vet Adv. 2010; 9: 2290-2294.
55. Padungtod P, Kaneene JB. Salmonella in food animals and humans in northern Thailand. Int J Food Microbiol. 2006; 108: 346-354.
56. Parveen S, Taabodi M, Schwarz JG, Oscar TP, Harter-Dennıs J, Whıte DG. Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. J Food Protec. 2007; 70: 2466-2472.
57. Pesavento G, Ducci B, Nieri D, Comodo N, Lo Nostro A. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control. 2010; 21: 708-713.
58. Rahimi E, Farzad Y, Farzinezhadizadeh H. Prevalence and antimicrobial resistance of Listeria species isolated from different types of raw meat in Iran. J Food Protec. 2012; 12: 2100-2304.
59. Reginato A, Pinheiro, Do Nascımento V, Oliveira M., Ruschel L, Da Silveira L. Utilization of immunomagnetic separation for detection of Salmonella in raw broiler parts. Braz J Microbiol. 2002; 33: 339-341.
60. Roy P, Dhillon AS, Lauerman LH, Schaberg DM, Bandli D, Johnson S. Results of Salmonella İsolation from poultry products, poultry, poultry environment, and other characteristics, Am Assoc Avian Pathol. 2002; 46(1): 17-24.
61. Ryser ET, Marth EH. Listeria, Listeriosis and Food Safety, 3 th Ed.,Taylor and Francis Group, Crc Press, Sound Parkway NW. 2007.
62. Soltan Dallal MM, Doyle MP, Rezadehbashi M, Dabiri H, Sanaei M, Modarresi S, Bakhtiari R, Sharifiy K, Taremi M, Zali MR, Sharifi-Yazdı MK. Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp., isolated from retail chicken and beef, Tehran, Iran. Food Control. 2010; 21: 388-392.
63. Sakaridis I, Soultos N, Iossıfidou E, Papa A, Ambrosiadis I, Koidis P. Prevalence and antimicrobial resistance of Listeria monocytogenes isolated in chicken slauughterhouses in Northern Greece. J Food Protec. 2011; 6: 872-1040.
64. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL. Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 2011; 17: 7-15.
65. Seong PN, Ch SH, Park KM, Kang GH, Park BY, Moon SS, Ba HV. Characterization of chicken by-products by mean of proximate and nutritional compositions. Korean J Food Sci An. 2015; 35:(2) 179-188.
66. Shelly R, Abiodun A, Zinora A, William S. Occurence of selected foodborne pathogens on poultry and poultry giblets from small retail processing oprerations in Trinidad. J Food Protec. 2006; 5: 1096-1105.
67. Shrestha A, Regmi P, Dutta RK, Khanal DR, Aryal SR, Thakur RP, Karki D, Singh UM. First report on antimicrobial resistance of Salmonella isolated from poultry in Nepal. Vet Microbiol. 2010; 144: 522-524.
68. Sinell HJ. Microflora of edible offal with particular referance to Salmonella. In: Kiss I, Deak T, Incze K, Ed., Microbial Associations and Interactions in Food. 12th International IUMS-ICFMH Symposium, Budapest, Hungary. 1983; pp. 37-42.
69. Sodagari HR, Mashak Z, Ghadımianazar A. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran. J Infect Dev Ctries. 2015; 9(5): 463-469.
70. Sommer Morten OA, Dantas G. Antibiotics and the resistant microbiome. Cur Opin Microbiol. 2011; 14: 556–563.
71. Srinivasan V, Nam HM, Nguyen LT, Tamılselvam B, Murinda SE, Oliver SP. Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Path Dis. 2005; 2: 201-211.
72. Stonsaovapak S, Boonyaratanakornkit B. Prevalence and antimicrobial resistance of Listeria species in food products in Bangkok, Thailand, J Food Safety. 2010; 30; 154-161.
73. Su LH, Chiu, CH, Chu CS, Ou JT. Antimicrobial resistance in non typhoid Salmonella serotppes: a global challenge. Clin Infect Dis. 2004; 39: 546-551.
74. Temelli S, Kahya S, Eyigor A, Çarlı KT. Antibiotic resistance phenotypes of Salmonella isolates of broiler meat and chicken origin. Ankara Üniv Vet Fak Derg. 2012; 59: 107-114. Tollefson LM, Miller A. Antibiotic use in food animals: controlling the human health impact, J AOAC Int. 2000; 83(2): 245-254.
75. Tonbak F, Atasever M, Çalıcıoğlu M. Kanatlı etlerinde Salmonella riski. Atatürk Üniv Vet Bilim Derg. 2017;12(1): 90–8.
76. ULLOA ,J., GONZALEZ ,M., HERNANDEZ, C., VILLANUEVA, MP., FERNANDEZ H. (2010). Salmonella Enteritidis in chicken carcasses and giblets in Southern Chile. J Infect Dev Ctries, 4(2): 107-109.
77. Van Duıjkeren E, Houwers DJ. A critical assessment of antimicrobial treatment in uncomplicated Salmonella Enteritidis. Vet Microbiol. 2000; 73: 61-75.
78. Walsh D, Duffy G, Sheridan JJ, Blair, IS, Mcdowell DA. Antibiotic resistance among Listeria, including Listeria monocytogenes in retail foods. J Appl Microbiol. 2001;.90: 517-22.
79. Wang J, Zheng RZ, Wang JY. Risk assessment of Salmonella in animal derived food. Clin J Animal Quarantine. 2007; 24: 23-25.
80. White DG, Zhao S, Simjee S, Wagner DD, Mcdermott PF. Antimicrobial resistance of foodborne pathogens. Microbes Infect. 2002; 4(4): 405-412.
81. Yang B, Qu D, Zhang X, Shen J, Cuı S, Shi Y, Xi M., Sheng M, Zhi S, Meng J. Prevalence and characterization of Salmonella serovars in retail meats of market place in Shaanxi, China. Int J Food Microbiol. 2010; 141:63-72.
82. Yıldırım Y, Gonulalan Z, Pamuk S, Ertas, N. Incidence and antibiotic resistance of Salmonella spp. on raw chicken carcasses. Food Res Int. 2011; 44: 725-728.