The use of antibiotics in food animals creates an important source of antimicrobial resistant bacteria that can spread to humans through the food chain. Strains of Salmonella spp. with resistance to antimicrobial drugs are now widespread in all countries. The present study analysed the prevalence and antimicrobial resistance of Salmonella spp. isolates in raw chicken wings. Out of 200 fresh raw chicken wing packages 102 (51%) samples were positive. Antibiotic resistance test was performed on 200 isolates out of 336 after being confirmed. All the isolates showed multiple resistance against the antibiotics investigated with the average 0.371 multiple antibiotic resistance (MAR) index. None of the isolates were resistant to amoxicillin/clavulanate and cefoxitin. Only 2 isolates showed intermediate resistance to imipenem. The major resistance was observed against nalidixic acid (95%), trimethoprim/sulfomethoxazole (92%), tetracycline (92%), streptomycin (90%) and trimethoprim (81%). Even though only 4 isolates were resistant against ciprofloxacin, high percentage of intermediate resistance (92%) was detected. Some of the isolates were also resistant to gentamicin (7%), cefoperazone (2%), ampicillin (24%), chloramphenicol (24%), cephazolin (7%) and cefotaxime (39%). According to our results high prevalence and the increase in antibiotic resistant Salmonella spp. is of concern and constitutes a threat to public health.
Gıda amaçlı hayvan yetiştiriciliğinde antibiyotik kullanımı, gıda zinciri yoluyla insana geçiş yapan, antibiyotiklere dirençli bakterilerin en önemli kaynağı konumundadır. Günümüzde antimikrobiyal ilaçlara dirençli Salmonella spp. tüm ülkelere yayılmış durumdadır. Bu çalışma ile kanatlı etlerindeki Salmonella prevalansı ve izolatların antimikrobiyal direnç durumları araştırılmıştır. İncelenen 200 piliç kanat paketinden 102 tanesi (%51) pozitif olarak değerlendirilmiş ve konfirme edilen 336 izolattan 200’ünün antibiyotik duyarlılık durumları belirlenmiştir. Buna göre tüm izolatların ortalama 0.371 çoklu antibiyotik direnci (MAR) indeksi ile çoklu antibiyotik direncine sahip olduğu görülmüştür. İzolatların hiçbiri amoxicillin/clavulanate ve cefoxitin’e direnç göstermemiştir. Yalnızca 2 izolatın imipenem’e dirençli olduğu saptanmıştır. Asıl direncin nalidixic acid (%95), trimethoprim/sulfomethoxazole (%92), tetracycline (%92), streptomycin (%90) ve trimethoprim (%81) antibiyotiklerine karşı şekillendiği gözlenmiştir. Her ne kadar sadece 4 izolat ciprofloxacin’e karşı tam dirençli olsa da orta düzeydeki direnç oranının yüksek olduğu (%92) ortaya konmuştur. İzolatlar ayrıca gentamisin (%7), cefoperazone (%2), ampicillin (%24), chloramphenicol (%24), cephazolin (%7) ve cefotaxime (%39)’e karşı direnç geliştirmiştir. Çalışmamızın bulguları Salmonella spp.’nin yüksek prevalansı ve antibiyotik direncindeki artış nedeniyle halk sağlığına yönelik önemli bir tehdit oluşturduğuna dikkati çekmiştir.
___
aradat ZW, Abedel Hafiz L, Ababneh MM, Ababneh QO, Al Mousa W, Al-Nabulsi A, Osaili TM, Holley R: Comparative analysis of virulence and resistance profiles of Salmonella enteritidis isolates from poultry meat and foodborne outbreaks in northern Jordan. Virulence, 5 (5): 601-610, 2014. DOI: 10.4161/viru.29002
Duffy G, Cloak OM, O’Sullivan MG, Guillet A, Sheridan JJ, Blair IS, McDowell DA: The incidence and antibiotic resistance profiles of Salmonella spp. on Irish retail meat products. Food Microbiol, 16, 623-631, 1999. DOI: 10.1006/fmic.1999.0278
Nguyen DTA, Kanki M, Nguyen PD, Le HT, Ngo PT, Tran DNM, Le NH, Dang CV, Kawai T, Kawahara R, Yonogi S, Hirai Y, Jinnai M, Yamasaki S, Kumeda Y, Yamamoto Y: Prevalence, antibiotic resistance, and extended-spectrum and AmpC b-lactamase productivity of Salmonella isolates from raw meat and seafood samples in Ho Chi Minh City, Vietnam. Int J Food Microbiol, 236, 115-122, 2016. DOI: 10.1016/j. ijfoodmicro.2016.07.017
Collignon P, Powers JH, Chiller TM, Aidara-Kane A, Aarestrup FM: World health organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin Infect Dis, 49 (1): 132-141, 2009. DOI: 10.1086/599374
Kaya İB, Şahan Yapıcıer Ö, Akan M, Diker KS: Class 1 integrons and the antibiotic resistance profile of Salmonella Infantis strains from broiler chickens. Kafkas Univ Vet Fak Derg, 23 (5): 803-807, 2017. DOI: 10.9775/ kvfd.2017.17821
Alcaine SD, Molla L, Nugen SR, Kruse H: Results of a pilot antibiotic resistance survey of Albanian poultry farms. J Glob Antimicrob Resist, 4, 60-64, 2016. DOI: 10.1016/j.jgar.2015.11.003
Zhu Y, Lai H, Zou L, Yin S, Wang C, Han X, Xia X, Hu K, He L, Zhou K, Chen S, Ao X, Liu S: Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. Int J Food Microbiol, 259, 43-51, 2017. DOI: 10.1016/j. ijfoodmicro.2017.07.023
Yildirim Y, Gonulalan Z, Pamuk S, Ertas N: Incidence and antibiotic resistance of Salmonella spp. on raw chicken carcasses. Food Res Int, 44 (3): 725-728, 2011. DOI: 10.1016/j.foodres.2010.12.040
Asif M, Rahman H, Qasim M, Khan TA, Ullah W, Jie Y: Molecular detection and antimicrobial resistance profile of zoonotic Salmonella enteritidis isolated from broiler chickens in Kohat, Pakistan. J Chin Med Assoc, 80 (5): 303-306, 2017. DOI: 10.1016/j.jcma.2016.11.007
Ziech RE, Lampugnani C, Perin AP, Sereno MJ, Sfaciotte RAP, Viana C, Soares VM, Pinto JPAN, Bersot LS: Multidrug resistance and ESBL-producing Salmonella spp., isolated from broiler processing plants. Braz J Microbiol, 47 (1): 191-195, 2016. DOI: 10.1016/j.bjm.2015.11.021
Álvarez-Fernández E, Alonso-Calleja C, García-Fernández C, Capita R: Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: Comparison between 1993 and 2006. Int J Food Microbiol, 153 (3): 281-287, 2012. DOI: 10.1016/j. ijfoodmicro.2011.11.011
Krumperman PH: Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of faecal contamination of foods. Appl Environ Microbiol, 46 (1): 165-170, 1983.
EUCAST, European Society of Clinical Microbiology and Infectious Diseases: European committee on antimicrobial susceptibility testing guidelines for detection resistance mechanisms and specific resistances of clinical and/or epidemiological importance. 2013.
CLSI: Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing: twenty-fourth informational supplement. CLSI document M100-S24. Wayne, PA: CLSI, 2014.
ISO, The International Organization of Standardizations: Microbiology of food animal feeding stuffs-horizontal method for the detection Salmonella spp. International Standard, ISO 6579.
Su LH, Chiu CH, Chu C, Ou JT: Antimicrobial resistance in nontyphoid Salmonella serotype: A global challenge. Clin Infect Dis, 39 (4): 546-551, 2004. DOI: 10.1086/422726
WHO: Global Strategy for containment of antimicrobial Resistance. WHO, Geneva. WHO/CDC/CSR/DR/2001.2, 2001.
Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG Jr: Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci USA, 99 (9): 6434-6439, 2002. DOI: 10.1073/pnas.082188899
Johnson JR, Kuskowski MA, Menard M, Gajewski A, Xercavins M, Garau J: Similarity between human and chicken Escherichia coli isolates in relation to Ciprofloxacin resistance status. J Infect Dis, 194, 71-78, 2006. DOI: 10.1086/504921
Aarestrup FM, Wegener HC, Collignon P: Resistance in bacteria of the food chain: Epidemiology and control strategies. Expert Rev Anti Infect Ther, 6 (5): 733-750, 2008. DOI: 10.1586/14787210.6.5.733
Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM: Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev, 28 (4): 901-937, 2015. DOI: 10.1128/CMR.00002-15
White DG, Zhao S, Sudler R, Ayers S, Friedman S, Chen S, McDermott PF, McDermott S, Wagner DD, Meng J: The isolation of antibiotic-resistant Salmonella from retail ground meats. N Engl J Med, 345, 1147-1154, 2001. DOI: 10.1056/NEJMoa010315
FAO/WHO Food and Agriculture Organisations and United Nations/World Health Organisation: Salmonella and campylobacter Chicken Meat: Meeting Report, Microbiological Risk Assessment Series, No: 19, Rome, 56 pp, 2009.
Hassan AHA, Salam HSH, Abdel-Latef GK: Serological identification and antimicrobial resistance of Salmonella isolates from broiler carcasses and human stools in Beni-Suef, Egypt. Beni-Suef Univ J Appl Sci, 5, 202-207, 2016. DOI: 10.1016/j.bjbas.2016.04.002