Occurrence and antimicrobial resistance of Salmonella enterica subsp. enterica serovars Typhimurium, Enteritidis, and Typhi isolated from chicken eggs and poultry products

Occurrence and antimicrobial resistance of Salmonella enterica subsp. enterica serovars Typhimurium, Enteritidis, and Typhi isolated from chicken eggs and poultry products

This study was carried out to detect the occurrence and antimicrobial resistance of Salmonella enterica subsp. enterica serovarsTyphimurium, Enteritidis, and Typhi in 252 samples including 100 chicken eggs, 60 processed poultry products (20 nuggets, 20 salami samples, 20 sausages), and 92 poultry giblets (50 livers and 42 gizzards). Salmonella spp. and serovars were identified by PCR. The antimicrobial susceptibility testing was performed by disk diffusion method. Forty-seven (31%) of 152 poultry products and 5 (5%) of 100 egg samples were positive for Salmonella spp. Salmonella spp. was positive in 3.3%, 5%, 18%, and 27% of chicken nugget, sausage, gizzard, and liver samples, respectively. S. Typhimurium and S. Enteritidis were detected in 21 (8.3%) of samples (11 liver, 4 gizzard, 3 sausage, 3 eggshell) and 2 (0.8%) of samples (2 liver), respectively. All strains isolated from eggs were resistant to erythromycin (100%). Resistance profiles of nalidixic acid (80.7%), tetracycline (76.9%), neomycin (69.2%), cefazolin (36.5%), ampicillin (17.3%), and amoxicillin/clavulanic acid (9.6%) were evident and 86.5% of isolates exhibited multidrug resistance. In conclusion, the contamination rate of Salmonella spp. and high antibiotic resistance profiles among the isolates could pose risks for consumers. Effective control programs must be followed in processing and handling.

___

  • 1. Iseri O, Erol I. Incidence and antibiotic resistance of Salmonellaspp in ground turkey meat. Brit Poultry Sci 2010; 51: 60-66.
  • 2. CDC. Surveillance for Foodborne Disease Outbreaks, United States, 2012: Annual Report. Atlanta, GA, USA: CDC; 2012.
  • 3. Abraham A, Al-Khaldi S, Assimon SA, Beaudry C, Benner RA. Bad Bug Book: Foodborne Pathogenic Microorganisms and Natural Toxins Handbook. Silver Springs, MD, USA: U.S. Food and Drug Administration; 2012.
  • 4. Vose D, Koupeev T, Mintiens K. A Quantitative Microbiological Risk Assessment of Salmonella spp. in Broiler (Gallus gallus) Meat Production. Technical Report Submitted to the EFSA. Parma, Italy: EFSA; 2010.
  • 5. Herikstad H, Motarjemi Y, Tauxe RV. Salmonella surveillance: a global survey of public health serotyping. Epidemiol Infect 2002; 129: 1-8.
  • 6. Dümen E, Aydın A, Ghassan I. 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.
  • 7. Zhao S, Datta AR, Ayers S, Friedman S, Walker RD, White DG. Antimicrobial-resistant Salmonella serovars isolated from imported foods. Int J Food Microbiol 2003; 84: 87-92.
  • 8. Chen S, Zhao S, White DG, Schroeder CM, Lu R, Yang H, McDermott PF, Ayers S, Meng J. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol 2004; 70: 1-7.
  • 9. Singh S, Yadav AS, Singh SM, Bharti P. Prevalence of Salmonellain chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Int 2010; 43: 2027-2030.
  • 10. International Standardization Organization (ISO). Microbiology of Food and Animal Feeding Stuffs-Horizontal Method for the Detection of Salmonella spp. International Standard (ISO 6579). Geneva, Switzerland: ISO; 2002.
  • 11. Aabo S, Rasmussen, OF, Rossen L, Sorensen PD, Olsen JE. Salmonella identification by the polymerase chain reaction. Mol Cell Probe 1993; 7: 171-178.
  • 12. de Freitas CG, Santana ÂP, da Silva PHC, Gonçalves VSP, Barros MDAF, Torres FA, Murata LS, Perecmanis S. PCR multiplex for detection of Salmonella Enteritidis, Typhi and Typhimurium and occurrence in poultry meat. Int J Food Microbiol 2010; 139: 15-22.
  • 13. Croci L, Delibato E, Volpe G, De Medici D, Palleschi G. Comparison of PCR, electrochemical enzyme-linked immunosorbent assays, and the standard culture method for detecting Salmonella in meat products. Appl Environ Microbial 2004; 70: 1393-1396.
  • 14. Clinical and Laboratory Standards Institute (CLSI). Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement. CLSI Document M100-S24. Wayne, PA, USA: Clinical and Laboratory Standards Institute; 2014.
  • 15. Gupta V, Ray P, Sharma M. Antimicrobial resistance pattern of Shigella and non-typhi Salmonella isolated from patients with diarrhoea. Indian J Med Res 1999; 109: 43-45.
  • 16. Samaha IA, Ibrahim HAA, Hamada MO. Isolation of some enteropathogens from retailed poultry meat in Alexandria Province. Alexandria Journal of Veterinary Sciences 2012; 37: 17-22.
  • 17. Karadal F, Ertas N, Hizlisoy H, Abay S, Al S. Prevalence of Escherichia coli O157: H7 and their verotoxins and Salmonellaspp. in processed poultry products. J Food Safety 2013; 33: 313-318.
  • 18. Sodagari HR, Mashak Z, Ghadimianazar A. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran. J Infect Dev Ctries 2015; 9: 463-469.
  • 19. Jerngklinchani J, Koowatananukul C, Daengprom K, Saitanu K. Occurrence of salmonellae in raw broilers and their products in Thailand. J Food Protect 1994; 57: 808-810.
  • 20. Molla B, Mesfin A. A survey of Salmonella contamination in chicken carcass and giblets in central Ethiopia. Rev Med Vet 2003; 154: 267-270.
  • 21. Abdellah C, Fouzia RF, Abdelkader C, Rachida SB, Mouloud Z. Prevalence and anti-microbial susceptibility of Salmonellaisolates from chicken carcasses and giblets in Meknès, Morocco. African J Microbiol Res 2009; 3: 215-219.
  • 22. Oral AI, Türkyılmaz S. Broyler iç organlarından Salmonellaenterica subsp. enterica serovar Enteritidis’in izolasyonu ve izole edilen suşların antibiyotiklere duyarlılıklarının belirlenmesi. Erciyes Üniv Vet Fak Derg 2008; 5: 27-33 (in Turkish).
  • 23. Bayhan Öktem A, Kaynak Onurdağ F, Er B, Demirhan B. A research of Salmonella spp. in egg and egg products and survival of Salmonella in different temperatures. Turkish J Pharm Sci 2009; 6: 147-154.
  • 24. Çakıroğlu HS, Gümüşsoy KS. Ankara Garnizonunda tüketime sunulan tavuk yumurtalarnın Salmonella spp. yönünden analizi. Sağlık Bilimleri Dergisi 2005; 14: 158-162 (in Turkish).
  • 25. Telo A, Bijo B, Sulaj K, Beli E. Occurrence of Salmonella spp. in imported eggs into Albania. Int J Food Microbiol 1999; 49: 69-171.
  • 26. Humphrey TJ, Whitehead A, Gawler AHL, Henley A, Rowe B. Numbers of Salmonella Enteritidis in the contents of naturally contaminated hens eggs. Epidemiol Infect 1991; 106: 489-496.
  • 27. El-Aziz DMA. Detection of Salmonella Typhimurium in retail chicken meat and chicken giblets. Asian Pac J Trop Biomed 2013; 3: 678-681.
  • 28. Kılınç Ü, Aydın F. Kayseri yöresindeki tavukçuluk işletmelerinden toplanan tavuklardan izole edilen Salmonellatürlerinin antibiyotiklere duyarlılıkları. Erciyes Üniv Sağ Bil Derg 2006; 15: 35-40 (in Turkish).
  • 29. Cardoso MO, Ribeiro AR, Santos LR, Pilotto F, Moraes HLS, Salle CTP, Rocha SLS, Nascimento VP. Antibiotic resistance in Salmonella Enteritidis isolated from broiler carcasses. Brazilian J Microbiol 2006; 37: 368-371.
  • 30. Yildirim 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.
Turkish Journal of Veterinary and Animal Sciences-Cover
  • ISSN: 1300-0128
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

Comparison of the efficiency of concentrated soluble recombinant phospholipase D and natural phospholipase D enzymes

Osman ERGANİŞ, Aslı SAKMANOĞLU

The effect of feeding Rhizopus oligosporus on growth performance, nutrient digestibility, blood profile, fecal microbiota, and fecal score in weanling pigs

Inho KIM, Jae Hong PARK, Hyeok Min YUN

Effect of some essential oils (Allium sativum L., Origanum majorana L.) and ozonated olive oil on the treatment of ear mites (Otodectes cynotis) in cats

Mustafa YİPEL, Abuzer ACAR, Fulya YİPEL ALTINOK

Effects of dietary chicken grill and sunflower seed oils on performance, egg yolk cholesterol level, biochemical parameters, and oxidant/antioxidant status of laying hens

Tülay BÜYÜKOĞLU, Mustafa Numan OĞUZ, Fatma KARAKAŞ OĞUZ

Protective effects of S-adenosylmethionine (SAMe) and silybin on hepatorenal and hemostatic functions in dogs with endotoxemia

Meriç KOCATÜRK, Zeki YILMAZ, Pınar LEVENT, Oya İNAN ERALP

Selecting Eimeria tenella-resistance markers by comparing resistant and susceptible groups of Jinghai Yellow chickens

Jingyu WANG, Jingjing ZHANG, Tingting AN, Mingming SUN, Yuxin LIN, Genxi ZHANG, Kaizhou XIE, Guojun DAI

Effect of dietary supplementation with different levels of inulin-typefructans on renal expression of aquaporin 2 of growing piglets

Katarzyna MICHALEK, Marta GRABOWSKA, Mariusz Tomasz SKOWRONSKI, Maria LASZCZYNSKA, Adam LEPCZYNSKI, Agnieszka HEROSIMCZYK

The determination of in vitro gas production and metabolizable energy value of rice straw treated with exogenous fibrolytic enzymes

Buğra GENÇ, Nurcan ÇETİNKAYA, Zehra SELÇUK, Mustafa SALMAN

Early pregnancy diagnosis using a commercial ELISA test based on pregnancy-associated glycoproteins in Holstein-Friesian heifers and lactating cows

Mehmet Osman ATLI, Mehmet Salih KAYA, Mehmet KÖSE, Eyyüp Hakan UÇAR, Faruk BOZKAYA, Hasan MUTLU

Circulating metabolic and reproductive hormone changes in laying hens kept under various heat-combating systems

Zia UR-RAHMAN, Muhammad Safdar ANJUM, Mansur Abdullah SANDHU, Anum SAFDAR