Prevalence, Serotype Diversity and Antibiotic Resistance of Salmonella Among Poultry Meat and Eggs in Turkiye: A Meta-analysis

Abstract

Poultry is a well-known reservoir for Salmonella, and therefore numerous outbreaks have been reported among poultry meat products and eggs. This study is aimed at determining the pooled prevalence, serotype diversity and antibiotic resistance profiles of Salmonella among poultry meat and eggs sold in Turkiye. For this purpose, international (Web of Science and PubMed) and national (ULAKBIM TR Index) electronic databases were searched using based on relevant keywords in English and Turkish, and out of 1,818 articles, 41 were deemed eligible for inclusion in this meta-analysis. The random effects model was accepted when a substantial heterogeneity was obtained according to Q statistics and the I2 value, however the fixed effects model was assumed valid in the opposite case. The pooled prevalence of Salmonella in chicken parts, chicken carcasses, chicken giblets and eggs were 24.4% [95% confidence interval (CI)=17.8-32.6], 21.9% (95% CI=14.0-32.7), 20.1% (95% CI=10.7-34.6) and 4.8% (95% CI=1.7-13.3), respectively. Salmonella Enteritidis was the most common serotype among eggs, chicken parts and chicken carcasses with the rates of 22.4% (95% CI=3.6-69.3), 19.0% (95% CI=3.3-61.6) and 5.8% (95% CI=2.2-14.4), respectively. The highest pooled antibiotic resistance prevalence of Salmonella spp., regardless of food type, was found in tetracycline (73.9%, 95% CI=51.0-88.5) (p<0.041) and ampicillin (31.5%, 95% CI=20.7-44.6). The high-pooled prevalence of the organism emphasized the potential threat Salmonella poses to public health, and also antibiotic resistance data revealed that the use of tetracyclines, quinolones and penicillin in poultry livestock should be restricted. These results will be of great use in the future epidemiological surveillance of Salmonella spp. presence and antibiotic resistance among poultry meat and eggs in Turkiye.

Keywords

• Salmonella
• Enteritidis
• Infantis
• Chicken
• Resistance
• Teyracycline
• Ampicillin

References

1. Agyare C, Boamah V E, Zumbi C N & Osei F B (2018). Antibiotic use in poultry production and its effects on bacterial resistance. In: Kumar Y (Ed.), Antimicrobial Resistance A Global Threat. IntechOpen. doi.org/10.5772/intechopen.79371
2. BESD-BIR (2021a). Türkiye kanatlı eti üretimi (Turkish poultry meat production). Retrieved on August, 17, 2021 from https://besd-bir.org/assets/uploaded/Tr-kanatli-eti-uretimi-ton2.pdf
3. BESD-BIR (2021b). Poultry meat consumption per capita in Turkey. Retrieved on August, 17, 2021 from https://besd-bir.org/assets/uploaded/Tr-kisi-basina-kanatli-eti-tuketimi2.pdf Accessed
4. Cardoso M J, Nicolau A I, Borda D, Nielsen L, Maia R L, Møretrø T, Ferreira V, Knochel S, Langsrud S & Teixeira P (2021). Salmonella in eggs: From shopping to consumption-A review providing an evidence-based analysis of risk factors. Comprehensive Reviews in Food Science and Food Safety 20(3): 2716-2741. doi.org/10.1111/1541-4337.12753.
5. CDC (Centers for Disease Control and Prevention) (1984). Poultry Giblet-associated Salmonellosis- Maine. Morbidity and mortality weekly report 33(44): 630-631. Retrieved on August, 17, 2021 from https://www.cdc.gov/mmwr/preview/mmwrhtml/00000433.htm
6. CDC (Centers for Disease Control and Prevention) (2012). Multistate outbreak of human Salmonella Heidelberg infections linked to «kosher broiled chicken livers» from Schreiber Processing Corporation (final update). Retrieved on August, 18, 2021 from https://www.cdc.gov/salmonella/2011/chicken-liver-1-11-2012.html
7. CDC (Centers for Disease Control and Prevention) (2021). Reports of selected Salmonella outbreak investigations. Retrieved on August, 16, 2021 from https://www.cdc.gov/salmonella/outbreaks.html
8. Cufaoglu G, Ambarcioglu P, & Ayaz N D (2021). Meta-analysis of the prevalence of Listeria spp. and antibiotic resistant L. monocytogenes isolates from foods in Turkey. LWT 144: 111210. doi.org/10.1016/j.lwt.2021.111210.

9. Diker K S, Göncüoğlu M, Şahin G, Akan M, Gürcan İ S, Müştak H K, Ayaz N D, Sarıçam S, Salar M Ö, Açıkalın H D, Ünal G, Çöven F, Dakman A, Gülaçtı İ & Uzunboy E N (2020). Base study for the establishment of national Salmonella control program in hatching farms and table eggs in Turkey. Turkish Journal of Veterinary & Animal Sciences 44(2): 343-349. doi.org/10.3906/vet-1908-2
10. EFSA (European Food Safety Authority) (2010). EFSA publishes survey on Campylobacter and Salmonella in chicken in the EU. Retrieved on August, on 26, 2021 from https://www.efsa.europa.eu/en/press/news/100317
11. EFSA & ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control) (2021a). The European Union One Health 2019 Zoonoses Report. EFSA Journal 19(2): 6406. doi.org/10.2903/j.efsa.2021.6406.
12. EFSA & ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control) (2021b). The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals, and food in 2018/2019. EFSA Journal 19(4): 6490. doi.org/10.2903/j.efsa.2021.6490.
13. European Parliament (2021). Motion for a resolution. Committee on the Environment, Public Health and Food Safety 2021/2718 (DEA). Retrieved from https://www.europarl.europa.eu/meetdocs/2014_2019/plmrep/COMMITTEES/ENVI/DV/2021/07-12/RE_Objection_DA_antimicrobials_2021_EN.pdf.
14. Ferrari R G, Rosario D K, Cunha-Neto A, Mano S B, Figueiredo E E & Conte-Junior C A (2019). Worldwide epidemiology of Salmonella serovars in animal-based foods a Meta-Analysis. Applied and Environmental Microbiology 85(14): e00591-19. doi.org/10.1128/AEM.00591-19. 
15. Golden C E & Mishra A (2020). Prevalence of Salmonella and Campylobacter spp. in alternative and conventionally produced chicken in the United States: A systematic review and Meta-Analysis. Journal of Food Protection 83(7): 1181-1197. doi.org/10.4315/JFP-19-538.
16. Gonçalves-Tenório A, Silva B N, Rodrigues V, Cadavez V, & Gonzales-Barron U (2018). Prevalence of pathogens in poultry meat: a meta-analysis of European published surveys. Foods 7(5): 69. doi.org/10.3390/foods7050069.
17. Higgins J P T & Thompson S G (2002). Quantifying heterogeneity in a Meta-Analysis. Statistics in Medicine 21(11): 1539-1558. doi.org/10.1002/sim.1186.
18. Hosseininezhad B, Berizi E, Nader M, Mazloomi S M, Hosseinzadeh S, Ebrahimi L & Zare M (2020). Prevalence of Salmonella contamination in consumed eggs in Iran: A systematic review and meta-analysis study on published studies from 1996 to 2018. Veterinary World 13(12): 2743-2751. doi.org/10.14202/vetworld.2020.2743-2751.
19. Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, de Pinna E, Nair S, Fields P I & Weill F X (2014). Supplement 2008-2010 (no. 48) to the white-Kauffmann-Le minor scheme. Research in Microbiology 165(7): 526-530. doi.org/10.1016/j.resmic.2014.07.004.
20. Lanier W A, Hale K R, Geissler A L & Dewey-Mattia D (2018). Chicken liver-associated outbreaks of Campylobacteriosis and Salmonellosis, United States, 2000-2016: identifying opportunities for prevention. Foodborne Pathogens and Disease 15(11): 726-733. doi.org/10.1089/fpd.2018.2489. 
21. Luber P (2009). Cross-contamination versus undercooking of poultry meat or eggs -which risks need to be managed first? International Journal of Food Microbiology 134: 21-28. doi.org/10.1016/j.ijfoodmicro.2009.
22. Mavridis D & Salanti G (2014). How to assess publication bias: funnel plot, trim-and-fill method and selection models. Evidence-Based Mental Health 17(1): 30. doi.org/10.1136/eb-2013-101699.
23. O’Neil J (2015). Tackling a global health crisis: initial steps/ the review on antimicrobial resistance. Retrieved on 26 August, 2021 from https://wellcomecollection.org/works/bfepg7pb/items
24. Patsopoulos N A, Evangelou E & Ioannidis J P A (2008). Sensitivity of between-study heterogeneity in meta-analysis: proposed metrics and empirical evaluation. International Journal of Epidemiology 37(5): 1148-1157. doi.org/10.1093/ije/dyn065.
25. Tadesse G & Gebremedhin E Z (2015). Prevalence of Salmonella in raw animal products in Ethiopia: a meta-analysis. BMC Research Notes 8(1): 1-8. doi.org/10.1186/s13104-015-1127-7.
26. The Food Safety and Inspection Service (2021). Chicken liver - resources for illness prevention. Retrieved on August, 26, 2021 from https://www.fsis.usda.gov/ChickenLiver.
27. Thomas K M, de Glanville W A, Barker G C, Benschop J, Buza J J, Cleaveland S, Davis M A, French N P, Mmbaga B T, Prinsen G, Swai E S, Zadoks R N & Crump J A (2020). Prevalence of Campylobacter and Salmonella in African food animals and meat: a systematic review and meta-analysis. International Journal of Food Microbiology 315: 108382. doi.org/10.1016/j.ijfoodmicro.2019.108382.
28. TUBITAK (The Scientific and Technological Research Council of Turkey) (2017). Development of control and monitoring program for Salmonella in poultry and poultry products. Project no: 113R036. Retrieved from https://app.trdizin.gov.tr/proje/TVRjMk1EQXc/kanatli-hayvanlardan-ve-gidalardan-salmonella-izlenmesi-ve-kontrol-programlarinin-gelistirilmesi
29. TUIK (Turkish Statistical Institute) (2021). Number of poultry animals by types. Retrieved on August, 27, 2021 from https://data.tuik.gov.tr/Bulten/Index?p=Poultry-Production-March-2021-37217&dil=2
30. Turkish Food Codex (2018). Türk gıda kodeksi mikrobiyolojik kriterler yönetmeliğinde değişiklik yapılmasına dair yönetmelik (Regulation on amending the Turkish food codex microbiological criteria regulation). Retrieved on October, 9, 2018, No: 30560, Ankara from https://www.resmigazete.gov.tr/eskiler/2018/10/20181009-2.htm
31. Voss-Rech D, Potter L, Vaz C S L, Pereira D I B, Sangioni L A, Vargas Á C & de Avila Botton S (2017). Antimicrobial resistance in nontyphoidal Salmonella isolated from human and poultry-related samples in Brazil: 20-year meta-analysis. Foodborne Pathogens and Disease 14(2): 116-124. doi.org/10.1089/fpd.2016.2228.
32. WHO (2018). Critically important antimicrobials for human medicine (6th revision). Retrieved from https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf.
33. YUM-BIR (2021). Sector data- 2018. Retrieved on August, 27, 2021 from https://www.yum-bir.org/yumurta/id30-istatistikler
34. Zelalem A, Sisay M, Vipham J L, Abegaz K, Kebede A & Terefe Y (2019). The prevalence and antimicrobial resistance profiles of bacterial isolates from meat and meat products in Ethiopia: a systematic review and meta-analysis. International Journal of Food Contamination 6(1): 1-14. doi.org/10.1186/s40550-019-0071-z.