Hafize Dilşad AÇIKALIN,
İrem GÜLGEÇTİ,
Merve ÖZDAL SALAR,
Mehmet Metin ÇİFTCİ,
Seden Arzu BİRİNCİ,
Gültekin ÜNAL,
Emine Nazan UZUNBOY,
Hamit Kaan MÜŞTAK,
Güzin ŞAHİN,
Mehmet AKAN,
Naim Deniz AYAZ,
Asiye DAKMAN,
İsmail Safa GÜRCAN,
Seyyide SARIÇAM,
Kadir Serdar DİKER,
Fethiye ÇÖVEN,
Kamile KESLER,
Hü
2321
Base study for the establishment of national Salmonella control program in hatching farms and table eggs in Turkey
Base study for the establishment of national Salmonella control program in hatching farms and table eggs in Turkey
Foodborne infections due to Salmonella are still a major concern worldwide. Particularly contaminated egg and egg relatedproducts are the primary sources for human salmonellosis. It is necessary to determine the risk factors associated with Salmonellacontamination of eggs within the scope of farm to table and environment. The objective of this study was to develop the “NationalSalmonella Control Program in Laying Hens” and report the prevalence and serotype distribution findings of Salmonella in laying hensand eggs in Turkey. A total of 2122 samples were collected and analysed according to ISO 6579:2002 after the isolation and identificationprocedures. All Salmonella isolates were serotyped including 726 eggs and 1396 farm specimens from 241 epidemiological units (EpUs)that were located in 9 different provinces between 2015 and 2017. Salmonella contamination was detected in 14.9% of 241 EpUs. Theresults indicated that almost half of the flocks have multiple contamination sources. The highest contamination rate was obtained fromenvironmental (11%) followed by faeces (7.5%) and the lowest was from water samples (1.6%). The overall contamination rate wasdetected as 7.46% for farms and 3.3% for eggs. As S. Enteritidis and S. Typhimurium are the most frequently seen serotypes all overthe world, in Turkey S. Typhimurium was not detected and S. Enteritidis was the 5th most common isolated serotype. According toour results it can be concluded that differences in various countries, particularly geographical and egg hatching systems, may affect thecontamination rate and serotype distribution of Salmonella.
___
- 1. TÜİK. Production of Poultry Meat Ankara, Turkey: TÜİK;
2018.
- 2. Yum-Bir. Yumurta Tavukçuluğu Verileri. Ankara, Turkey:
Yum-Bir; 2018.
- 3. Pires SM, Vieira AR, Hald T, Cole D. Source attribution of
human Salmonellosis: an overview of methods and estimates.
Foodborne Pathogens and Disease 2014; 11: 667-676.
- 4. Magwedere K, Rauff D, De Klerk G, Keddy KH, Dziva F.
Incidence of nontyphoidal Salmonella in food-producing
animals, animal feed, and the associated environment in
South Africa, 2012-2014. Clinical Infectious Diseases 2015; 61:
S283-S289.
- 5. Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J et al.
Population dynamics of Salmonella enterica serotypes
in commercial egg and poultry production. Applied and
Environmental Microbiology 2011; 77: 4273-4279.
- 6. Crim SM, Iwamoto M, Huang JY, Griffin PM, Gilliss D et al.
Incidence and trends of infection with pathogens transmitted
commonly through food - foodborne diseases active
surveillance network, 10 US sites, 2006-2013. Morbidity and
Mortality Weekly Report 2014; 63: 328-332.
- 7. CDC (Centers for Disease Control and Prevention). Outbreaks
of Salmonella serotype Enteritidis infection associated with
eating shell eggs-United States, 1999–2001. Morbidity and
Mortality Weekly Report 2003; 51 (51): 1149-1152.
- 8. Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. Outbreakassociated
Salmonella enterica serotypes and food commodities,
United States, 1998-2008. Emerging Infectious Diseases Journal
2013; 19: 1239-1244.
- 9. Whiley H, Ross K. Salmonella and eggs: from production to plate.
International Journal of Environmental Research and Public
Health 2015; 12: 2543-2556.
- 10. De Reu K, Grijspeerdt K, Messens W, Heyndrickx A, Uyttendaele
M et al. Eggshell factors influencing eggshell penetration and whole
egg contamination by different bacteria, including Salmonella
Enteritidis. International Journal of Food Microbiology 2006;
112: 253-260.
- 11. Gole VC, Caraguel CGB, Sexton M, Fowler C, Chousalkar KK.
Shedding of Salmonella in single age caged commercial layer flock
at an early stage of lay. International Journal of Food Microbiology
2014; 189: 61-66.
- 12. Im MC, Jeong SJ, Kwon YK, Jeong OM, Kang MS et al. Prevalence
and characteristics of Salmonella spp. isolated from commercial
layer farms in Korea. Poultry Science 2015; 94: 1691-1698.
- 13. Gole VC, Torok V, Sexton M, Caraguel CGB, Chousalkar KK.
Association between indoor environmental contamination by
Salmonella enterica and contamination of eggs on layer farms.
Journal of Clinical Microbiology 2014; 52: 3250-3258.
- 14. Hoszowski A, Wasyl D. Typing of Salmonella enterica subsp
enterica serovar Mbandaka isolates. Veterinary Microbiology
2001; 80: 139-148.
- 15. Little CL, Walsh S, Hucklesby L, Surman-Lee S, Pathak K et al.
Survey of Salmonella contamination of non-united kingdomproduced
raw shell eggs on retail sale in the northwest of England
and London, 2005 to 2006. Journal of Food Protection 2007; 70:
2259-2265.
- 16. Denagamage T, Jayarao B, Patterson P, Wallner-Pendleton E,
Kariyawasam S. Risk factors associated with Salmonella in laying
hen farms: systematic review of observational studies. Avian
Disease 2015; 59: 291-302.
- 17. EFSA (European Food Safety Authority). Multi-country outbreak
of Salmonella Enteritidis infections associated with consumption
of eggs from Germany. EFSA Supporting Publication 2014. doi:
10.2903/sp.efsa.2014.en-646
- 18. EFSA (European Food Safety Authority). Scientific opinion on a
quantitative estimation of the public health impact of setting a
new target for the reduction of Salmonella in laying hens. EFSA
Journal 2010; 8 (4): 1546.
- 19. European Commission. Commission regulation (EU) No
517/2011 of 25 May 2011 implementing Regulation No
2160/2003 of the European Parliament and of the Council as
regards a Union target for the reduction of the prevalence of
certain Salmonella serotypes in laying hens of Gallus gallus and
amending Regulation (EC) No 2160/2003 and Commission
Regulation (EU) No 200/2010. Official Journal of the European
Union 2018; 138: 45-51.
- 20. European Commission. Commission Regulation (EC) No
152/2009 of 27 January 2009 laying down the methods of sampling
and analysis for the official control of feed. Official Journal of the
European Union 2009; 54: 1-130.
- 21. Cıngı H. Örnekleme Kuramı/Sampling Theory. 3rd ed. Ankara,
Turkey: Hacettepe Üniversitesi Fen Fakültesi Matbaası; 2009
(in Turkish).
- 22. ISO 6579:2002 (E). Microbiology of Food and Animal Feeding
Stuffs-Horizontal Method for the Detection of Salmonella spp.
4rd ed. Geneva, Switzerland: ISO; 2002.
- 23. Grimont PAD, Weill FX. Antigenic formulae of the Salmonella
serovars. 9th ed. Paris, France: WHO Collaborating Centre for
Reference and Research on Salmonella, Institute Pasteur, 2007.
- 24. EFSA. Report of the task force on zoonoses data collection
on the analysis of the baseline study on the prevalence of
Salmonella in holdings of laying hen flocks of Gallus gallus.
EFSA Journal 2007; 97.
- 25. Rajan K, Shi Z, Ricke SC. Current aspects of Salmonella
contamination in the US poultry production chain and the
potential application of risk strategies in understanding
emerging hazards. Critical Reviews in Microbiology 2017; 43
(3): 370-392.
- 26. Iwabuchi E, Maruyama N, Hara A, Nıshimura M, Muramatsu
M et al. Nationwide survey of Salmonella prevalence in
environmental dust from layer farms in Japan. Journal of Food
Protection 2010; 73 (11): 1993-2000.
- 27. FDA. NARMS -The National Antimicrobial Resistance
Monitoring System. Washington, DC, USA: FDA; 2014.
- 28. Erol I, Goncuoglu M, Ayaz ND, Ellerbroek L, Ormanci FSB
et al. Serotype distribution of Salmonella isolates from turkey
ground meat and meat parts. Biomed Research International
2013; 281591.
- 29. Goncuoglu M, Ormanci FSB, Uludag M, Cil GI. Prevalence
and antibiotic resistance of Salmonella spp. and Salmonella
Typhimurium in broiler carcasses wings and liver. Journal of
Food Safety 2016; 36: 524-531.
- 30. Kahya S, Eyigör A, Carlı KT. Comparison of different sample
types for Salmonella detection from chicken layer breeder
flocks. Uludağ University Journal of the Faculty of Veterinary
Medicine 2013; 32 (2): 19-24.
- 31. Ata Z, Aydin N. Isolation of Salmonella spp. from poultry
enterprises in Ankara region. Veterinary Journal of Ankara
University 2008; 55: 161-166.
- 32. Çakıroğlu HS, Gümüşsoy KS. Analysis of Salmonella spp.
contamination in chicken eggs served for consumption in
Ankara Garrison. Journal of Health Sciences 2005; 14 (3): 158-
162.
- 33. Chousalkar K, Gast R, Martelli F, Pande V. Review of eggrelated
salmonellosis and reduction strategies in United States,
Australia, United Kingdom and New Zealand. Critical Reviews
in Microbiology 2018; 44: 290-303.
- 34. Gast RK, Guraya R, Guard-Bouldin J, Holt PS, Moore RW.
Colonization of specific regions of the reproductive tract
and deposition at different locations inside eggs laid by hens
infected with Salmonella Enteritidis or Salmonella Heidelberg.
Avian Disease 2007; 51: 40-44.