Skip to main content Accessibility help
×
Home

Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China

  • X. REN (a1), M. LI (a1), C. XU (a1), K. CUI (a1), Z. FENG (a1), Y. FU (a1), J. ZHANG (a1) and M. LIAO (a1)...

Summary

A total of 1145 samples were collected from chicken breeder farms, hatcheries, broiler farms, a slaughterhouse and retail refrigerated chicken stores in an integrated broiler supply chain in Guangdong Province, China, in 2013. One-hundred and two Salmonella enterica strains were isolated and subjected to serotyping, antimicrobial susceptibility testing, virulence profile determination and molecular subtyping by pulsed field gel electrophoresis (PFGE). The contamination rates in samples from breeder farms, hatcheries, broiler farms, the slaughterhouse and retail stores were 1·46%, 4·31%, 7·00%, 62·86% and 54·67%, respectively. The isolated strains of S. enterica belonged to 10 serotypes; most of them were S. Weltevreden (46·08%, 47/102) and S. Agona (18·63%, 19/102). Isolates were frequently resistant to streptomycin (38·2%), tetracycline (36·3%), sulfisoxazole (35·3%) and gentamicin (34·3%); 31·4% of isolates were multidrug resistant. The isolates were screened for 10 virulence factors. The Salmonella pathogenicity island genes avrA, ssaQ, mgtC, siiD, and sopB and the fimbrial gene bcfC were present in 100% of the strains. PFGE genotyping of the 102 S. enterica isolates yielded 24 PFGE types at an 85% similarity threshold. The PFGE patterns show that the genotypes of S. enterica in the production chain are very diverse, but some strains have 100% similarity in different parts of the production chain, which indicates that some S. enterica persist throughout the broiler supply chain.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China
      Available formats
      ×

Copyright

Corresponding author

*Authors for correspondence: Professor M. Liao, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Tianhe District, Guangzhou 510642, China. (Email: mliao@scau.edu.cn)

References

Hide All
1. Scallan, E, et al. Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases 2011; 17: 715.
2. Mao, XD, Jun-Feng, HU. Estimation on disease burden of foodborne non-typhoid salmonellosis in China using literature review method. Chinese Journal of Disease Control & Prevention 2011; 15: 622625.
3. Jackson, BR, et al. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerging Infectious Diseases 2013; 19:12391244.
4. Foley, SL, et al. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Applied and Environmental Microbiology 2011; 77: 42734279.
5. Löfström, C, et al. Outbreak of Salmonella enterica serovar Typhimurium phage type DT41 in Danish poultry production. Veterinary Microbiology 2015; 178: 167172.
6. Chao, MR, et al. Assessing the prevalence of Salmonella enterica in poultry hatcheries by using hatched eggshell membranes. Poultry Science 2007; 86: 16511655.
7. Logue, CM, et al. The incidence of antimicrobial-resistant Salmonella spp. on freshly processed poultry from US Midwestern processing plants. Journal of Applied Microbiology 2003; 94: 1624.
8. IATP. Institute for Agriculture and Trade Policy 2014. Fair or fowl? Industrialization of poultry production in China (http://www.iatp.org/files/2014_02_25_PoultryReport_f_web.pdf).
9. Visscher, CF, et al. Serodiversity and serological as well as cultural distribution of Salmonella on farms and in abattoirs in Lower Saxony, Germany. International Journal of Food Microbiology 2011; 146: 4451.
10. Gong, J, et al. Prevalence and fimbrial genotype distribution of poultry Salmonella isolates in China (2006 to 2012). Applied Environmental Microbiology 2014; 80: 687693.
11. Yang, B, et al. Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. International Journal of Food Microbiology 2010; 141: 6372.
12. Popoff, MY, et al. Supplement 2002 (no. 46) to 417 the Kauffmann–White scheme. Research in Microbiology 2004; 155: 568570.
13. CLSI. Performance standards for antimicrobial disk susceptibility tests, CLSI document M02-A10. Clinical and Laboratory Standards Institute, 2009.
14. CLSI. Performance standards for antimicrobial susceptibility testing; 20th informational supplement, CLSI document M100-S20. Clinical and Laboratory Standards Institute, 2010.
15. Ribot, EM, et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathogens and Disease 2006; 3: 5967.
16. Van Der Fels-Klerx, HJ, et al. Prevalence of Salmonella in the broiler supply chain in The Netherlands. Journal of Food Protection 2008; 71: 19741980.
17. Heyndrickx, M, et al. Routes for salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 2002; 129: 253265.
18. Lai, J, et al. Serotype distribution and antibiotic resistance of Salmonella in food-producing animals in Shandong province of China, 2009 and 2012. International Journal of Food Microbiology 2014; 180: 3038.
19. Berghaus, RD, et al. Multilevel analysis of environmental Salmonella prevalences and management practices on 49 broiler breeder farms in four south-eastern States, USA. Zoonoses Public Health 2012; 59: 365374.
20. Lu, Y, et al. Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China. Foodborne Pathogens and Disease 2011; 8: 4553.
21. Schwaiger, K, et al. Prevalence of antibiotic-resistant Enterobacteriaceae isolated from chicken and pork meat purchased at the slaughterhouse and at retail in Bavaria, Germany. International Journal of Food Microbiology 2012; 154: 206211.
22. van Asselt, ED, et al. Salmonella serotype distribution in the Dutch broiler supply chain. Poultry Science 2009; 88: 26952701.
23. Li, R, et al. Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China. International Journal of Food Microbiology 2013; 163: 1418.
24. Zhu, J, et al. Prevalence and quantification of Salmonella contamination in raw chicken carcasses at the retail in China. Food Control 2014; 44: 198202.
25. Marin, C, et al. Sources of Salmonella contamination during broiler production in Eastern Spain. Preventive Veterinary Medicine 2011; 98: 3945.
26. Choi, SW, et al. Prevalence and characterization of Salmonella species in entire steps of a single integrated broiler supply chain in Korea. Poultry Science 2014; 93: 12511257.
27. Nakao, JH, et al. ‘One Health’ investigation: outbreak of human Salmonella Braenderup infections traced to a mail-order hatchery – United States, 2012–2013. Epidemiology and Infection 2015; 143: 21782186.
28. Heyndrickx, M, et al. Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiology and Infection 2002; 129: 253265.
29. Gong, J, et al. Prevalence and fimbrial genotype distribution of poultry Salmonella isolates in China (2006 to 2012). Applied Environmental Microbiology 2014; 80: 687693.
30. Liang, Z, et al. Serotypes, seasonal trends, and antibiotic resistance of non-typhoidal Salmonella from human patients in Guangdong Province, China, 2009–2012. BMC Infectious Diseases. 2015; 15: 53.
31. Bangtrakulnonth, A, et al. Salmonella serovars from humans and other sources in Thailand, 1993–2002. Emerging Infectious Diseases 2004; 10: 131136.
32. Utrarachkij, F, et al. Possible horizontal transmission of Salmonella via reusable egg trays in Thailand. International Journal of Food Microbiology 2012; 154: 7378.
33. Ponce, E, et al. Prevalence and characterization of Salmonella enterica serovar Weltevreden from imported seafood. Food Microbiology 2008; 25: 2935.
34. Brankatschk, K, et al. Genome of a European fresh-vegetable food safety outbreak strain of Salmonella enterica subsp. enterica serovar Weltevreden. Journal of Bacteriology 2011; 193: 2066.
35. Alali, WQ, et al. Prevalence and distribution of Salmonella in organic and conventional broiler poultry farms. Foodborne Pathogens and Disease 2010; 7: 13631371.
36. Poros-Gluchowska, J, Markiewicz, Z. Antimicrobial resistance of Listeria monocytogenes. Acta Microbiologica Polonica 2003; 52: 113129.
37. Barbosa, TM, Levy, SB. The impact of antibiotic use on resistance development and persistence. Drug Resistance Updates 2000; 3: 303311.
38. Diarra, MS, et al. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Applied and Environmental Microbiology 2007; 73: 65666576.
39. Lu, Y, et al. Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China. Foodborne Pathogens and Disease 2011; 8: 4553.
40. Zhang, J, et al. Laboratory monitoring of bacterial gastroenteric pathogens Salmonella and Shigella in Shanghai, China 2006–2012. Epidemiology and Infection. 2015; 143: 478485.
41. Osman, KM, Hassan, WM, Mohamed, RA. The consequences of a sudden demographic change on the seroprevalence pattern, virulence genes, identification and characterisation of integron-mediated antibiotic resistance in the Salmonella enterica isolated from clinically diarrhoeic humans in Egypt. European Journal of Clinical Microbiology Infectious Diseases 2014; 33: 13231337.
42. Hapfelmeier, S, et al. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infection and Immunity 2004; 72: 795809.
43. Aslanzadeh, J, Paulissen, LJ. Adherence and pathogenesis of Salmonella enteritidis in mice. Microbiology and Immunology 1990; 34: 885893.
44. Guiney, DG, et al. Plasmid-mediated virulence genes in non-typhoid Salmonella serovars. FEMS Microbiology Letters 1994; 124: 19.
45. Lynne, AM, et al. Characterization of antimicrobial resistance in Salmonella enterica serotype Heidelberg isolated from food animals. Foodborne Pathogens and Disease 2009; 6: 207215.
46. Prager, R, et al. Prevalence and polymorphism of genes encoding translocated effector proteins among clinical isolates of Salmonella enterica . International Journal of Medical Microbiology 2000; 290: 605617.
47. Soto, SM, et al. Detection of virulence determinants in clinical strains of Salmonella enterica serovar Enteritidis and mapping on macrorestriction profiles. Journal of Medical Microbiology 2006; 55: 365373.
48. Mikasova, E, et al. Characterization of Salmonella enterica serovar Typhimurium strains of veterinary origin by molecular typing methods. Veterinary Microbiology 2005; 109: 113120.
49. Herrero, A, et al. Molecular epidemiology of emergent multidrug-resistant Salmonella enterica serotype Typhimurium strains carrying the virulence resistance plasmid pUO-StVR2. Journal of Antimicrobial Chemotherapy 2006; 57: 3945.
50. Chiu, CH, Ou, JT. Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. Journal of Clinical Microbiology 1996; 34: 26192622.
51. Huehn, S, et al. Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathogens and Disease 2010; 7: 523535.

Keywords

Related content

Powered by UNSILO

Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China

  • X. REN (a1), M. LI (a1), C. XU (a1), K. CUI (a1), Z. FENG (a1), Y. FU (a1), J. ZHANG (a1) and M. LIAO (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.