Skip to main content

Advertisement

SpringerLink
Log in

Molecular Epidemiology of Nontyphoidal Salmonella in Poultry and Poultry Products in India: Implications for Human Health

  • Original Article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Human infections with non-typhoidal Salmonella (NTS) serovars are increasingly becoming a threat to human health globally. While all motile Salmonellae have zoonotic potential, Salmonella Enteritidis and Salmonella Typhimurium are most commonly associated with human disease, for which poultry are a major source. Despite the increasing number of human NTS infections, the epidemiology of NTS in poultry in India has not been fully understood. Hence, as a first step, we carried out epidemiological analysis to establish the incidence of NTS in poultry to evaluate the risk to human health. A total of 1215 samples (including poultry meat, tissues, egg and environmental samples) were collected from 154 commercial layer farms from southern India and screened for NTS. Following identification by cultural and biochemical methods, Salmonella isolates were further characterized by multiplex PCR, allele-specific PCR, enterobacterial repetitive intergenic consensus (ERIC) PCR and pulse field gel electrophoresis (PFGE). In the present study, 21/1215 (1.73 %) samples tested positive for NTS. We found 12/392 (3.06 %) of tissue samples, 7/460 (1.52 %) of poultry products, and 2/363 (0.55 %) of environmental samples tested positive for NTS. All the Salmonella isolates were resistant to oxytetracycline, which is routinely used as poultry feed additive. The multiplex PCR results allowed 16/21 isolates to be classified as S. Typhimurium, and five isolates as S. Enteritidis. Of the five S. Enteritidis isolates, four were identified as group D Salmonella by allele-specific PCR. All of the isolates produced different banding patterns in ERIC PCR. Of the thirteen macro restriction profiles (MRPs) obtained by PFGE, MRP 6 was predominant which included 6 (21 %) isolates. In conclusion, the findings of the study revealed higher incidence of contamination of NTS Salmonella in poultry tissue and animal protein sources used for poultry. The results of the study warrants further investigation on different type of animal feed sources, food market chains, processing plants, live bird markets etc., to evaluate the risk factors, transmission and effective control measures of human Salmonella infection from poultry products.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bakeri SA, Yasin RM, Koh YT et al (2003) Genetic diversity of human isolates of Salmonella enterica serovar Enteritidis in Malaysia. J Appl Microbiol 95:773–780

    Article  CAS  PubMed  Google Scholar 

  2. Bhowmick PP, Srikumar S, Devegowda D et al (2012) Serotyping and molecular characterization for study of genetic diversity among seafood associated nontyphoidal Salmonella serovars. Indian J Med Res 135:371–381

    PubMed Central  PubMed  Google Scholar 

  3. Varga C, Pearl DL, McEwen SA et al (2013) Incidence, distribution, seasonality, and demographic risk factors of Salmonella Enteritidis human infections in Ontario, Canada, 2007–2009. BMC Infect Dis 13:212

  4. Gast RK, Guraya R, Guard J (2013) Salmonella enteritidis deposition in eggs after experimental infection of laying hens with different oral doses. J Food Prot 76:108–113

    Article  PubMed  Google Scholar 

  5. Grimont PA, Weill F (2007) Antigenic formulae of the Salmonella serovars, 9th edn. World Health Organization Collaborating Centre for Reference and Research on Salmonella, Institute Pasteur, Paris

    Google Scholar 

  6. Gast R (2003) Paratyphoid infections. In: Saif M, Barnes HJ, Fadly AM, Glisson JR, McDougald LR, Swayne DE (eds) Poult, 11th edn. Iowa State University Press, Ames, pp 583–613

  7. Breuil J, Brisabois A, Casin I et al (2000) Antibiotic resistance in salmonellae isolated from humans and animals in France: comparative data from 1994 and 1997. J Antimicrob Chemother 46:965–971

    Article  CAS  PubMed  Google Scholar 

  8. CDC (1997) Multidrug resistant Salmonella serovar Typhimurium—United States, 1996. Morb Mort Wkly Rep 46:308–310

    Google Scholar 

  9. Davis MA, Hancock DD, Besser TE et al (1999) Changes in antimicrobial resistance among Salmonella enterica Serovar typhimurium isolates from humans and cattle in the Northwestern United States, 1982–1997. Emerg Infect Dis 5:802–806

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Hatha AAM, Lakshmanaperumalsamy P (1997) Prevalence of Salmonella in fish and crustaceans in Coimbatore, South India. Food Microbiol 14:111–116

    Article  Google Scholar 

  11. Suresh T, Srinivasan D, Hatha AAM, Lakshmanaperumalsamy P (2000) A study on the incidence, antimicrobial resistance and survival of Salmonella and E. coli isolated from broiler chicken retail outlets. Microbes Environ 15:173–181

    Article  Google Scholar 

  12. Gopala Krishna Murthy T, Srinivasan P, Saravanan S, Mohan B (2011) Salmonella contamination in poultry. Indian Vet J 88:147–148

    Google Scholar 

  13. Murugadas V (2008) Molecular characterization of Salmonella enterica subsp. enterica from poultry and its products. M.V.Sc. thesis, Tamil Nadu Veterinary and Animal Sciences University

  14. Purushothaman V, David P, Venkatesan R (1996) Comparison of plasmid profile analysis, serotyping, resistotyping, biotyping and antimicrobial susceptibility testing as epidemiological tools in the strain identification of Salmonella isolates from avian source. Indian J Anim Sci 66:419–430

    Google Scholar 

  15. Bauer R, Kirby MDK, Sherris JC, Turck M (1996) Antibiotic susceptibility testing by standard single disc diffusion method. Am J Clin Pathol 14:493–496

    Google Scholar 

  16. Cortez ALL, Carvalho ACFB, Ikuno AA et al (2006) Identification of Salmonella spp. isolates from chicken abattoirs by multiplex-PCR. Res Vet Sci 81:340–344

    Article  CAS  PubMed  Google Scholar 

  17. Shah DH, Park J-H, Cho M-R et al (2005) Allele-specific PCR method based on rfbS sequence for distinguishing Salmonella gallinarum from Salmonella pullorum: serotype-specific rfbS sequence polymorphism. J Microbiol Methods 60:169–177

    Article  CAS  PubMed  Google Scholar 

  18. Cao S-Y, Wang M-S, Cheng A-C et al (2008) Comparative analysis of intestinal microbial community diversity between healthy and orally infected ducklings with Salmonella enteritidis by ERIC-PCR. World J Gastroenterol (WJG) 14:1120–1125

    Article  CAS  Google Scholar 

  19. Seo Y-S, Lee S-H, Shin E-K et al (2006) Pulsed-field gel electrophoresis genotyping of Salmonella gallinarum and comparison with random amplified polymorphic DNA. Vet Microbiol 115:349–357

    Article  CAS  PubMed  Google Scholar 

  20. Myint M (2004) Epidemiology of Salmonella contamination of poultry products: knowledge gaps in the farm to store products. Discussion submitted to Faculty of the Graduate School of University of Maryland, College Park

  21. Davies R, Breslin M (2003) Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Vet Rec 152:283–287

    Article  CAS  PubMed  Google Scholar 

  22. CDC (2011) Multistate outbreak of human salmonella heidelberg infections linked to “kosher broiled chicken livers” from Schreiber processing corporation. http://www.cdc.gov/salmonella/heidelberg-chickenlivers/111011/index.html?s_cid=ccu112111_015

  23. Islam M, Das B, Hossain K et al (2003) A study of the occurrence of poultry diseases in sylhet region of Bangladesh. Int J PoultSci 2:354–356

    Google Scholar 

  24. Okoli I, Endujihe G, Ogbuewu I (2006) Frequency of isolation of Salmonella from commercial poultry feeds and their anti microbial resistance profiles. Online J Health Allied Sci 5:2–3

    Google Scholar 

  25. Veldman A, Vahl HA, Borggreve GJ, Fuller DC (1995) A survey of the incidence of Salmonella species and Enterobacteriaceae in poultry feeds and feed components. Vet Rec 136:169–172

    Article  CAS  PubMed  Google Scholar 

  26. Ward J, Griffin M, Egan J (1996) Evaluation of some rapid methods for the detection of Salmonella in poultry carcasses, feed and environmental samples. In: Proceedings of the monit. proced. rapid. detect. methods tech., Newbury, UK, pp 123–127

  27. Wales A, Breslin M, Davies R (2006) Semiquantitative assessment of the distribution of Salmonella in the environment of caged layer flocks. J Appl Microbiol 101:309–318

    Article  CAS  PubMed  Google Scholar 

  28. Angen O, Skov M, Chriel M et al (1996) A retrospective study on Salmonella infection in Danish broiler flocks. Prev Vet Med 26:223–237

    Article  Google Scholar 

  29. Davies RH, Nicholas RA, McLaren IM et al (1997) Bacteriological and serological investigation of persistent Salmonella enteritidis infection in an integrated poultry organisation. Vet Microbiol 58:277–293

    Article  CAS  PubMed  Google Scholar 

  30. Carrique-Mas JJ, Breslin M, Snow L et al (2009) Persistence and clearance of different Salmonella serovars in buildings housing laying hens. Epidemiol Infect 137:837–846

    Article  CAS  PubMed  Google Scholar 

  31. Gilchrist MJ, Greko C, Wallinga DB et al (2007) The potential role of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance. Environ Health Perspect 115:313–316

    Article  PubMed Central  PubMed  Google Scholar 

  32. Threlfall EJ, Frost JA (1990) The identification, typing and fingerprinting of Salmonella: laboratory aspects and epidemiological applications. J Appl Bacteriol 68:5–16

    Article  CAS  PubMed  Google Scholar 

  33. Boxrud D, Pederson-Gulrud K, Wotton J et al (2007) Comparison of multiple-locus variable-number tandem repeat analysis, pulsed-field gel electrophoresis, and phage typing for subtype analysis of Salmonella enterica serotype Enteritidis. J Clin Microbiol 45:536–543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Torpdahl M, Sørensen G, Lindstedt B-A, Nielsen EM (2007) Tandem repeat analysis for surveillance of human Salmonella Typhimurium infections. Emerg Infect Dis 13:388–395

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Verma N, Reeves P (1989) Identification and sequence of rfbS and rfbE, which determine antigenic specificity of group A and group D salmonellae. J Bacteriol 171:5694–5701

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Desai AR, Shah DH, Shringi S et al (2005) An allele-specific PCR assay for the rapid and serotype-specific detection of Salmonella pullorum. Avian Dis 49:558–561

    Article  PubMed  Google Scholar 

  37. Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Saxena MK, Singh VP, Lakhcharua BD et al (2002) Strain differentiation of Indian isolates of Salmonella by ERIC-PCR. Res Vet Sci 73:313–314

    Article  CAS  PubMed  Google Scholar 

  39. Dionisi A, Carattoli A, Luzzi I et al (2006) Molecular genotyping of Salmonella abortionist by pulse field gel electrophoresis. Vet Microbiol 116:217–223

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are thankful to the Tamil Nadu Veterinary and Animal Sciences University for financial support and The University of Nottingham (S.V.K. and R.A.) for technical input into this research work.

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Poultry Disease Diagnosis and Surveillance Laboratory, Veterinary College and Research Institute Campus, Tamil Nadu Veterinary and Animal Sciences University, Namakkal, 637 002, Tamil Nadu, India

    Sellappan Saravanan, Thippichettypalayam Ramasamy Gopala Krishna Murthy, Palani Srinivasan, Vasudevan Gowthaman & Mohan Balusamy

  2. Centre for Animal Health Studies, Madhavarum Milk Colony, Tamil Nadu Veterinary and Animal Sciences University, Chennai, 600 0051, India

    Venketaraman Purushothaman

  3. Department of Veterinary Microbiology, Veterinary College and Research Institute, Tamil Nadu Veterinary and Animal Sciences University, Namakkal, 637 002, Tamil Nadu, India

    Kuppannan Sukumar

  4. School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, College Road, Loughborough, Leicestershire, LE12 5RD, UK

    Robert Atterbury & Suresh V. Kuchipudi

Authors
  1. Sellappan Saravanan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Venketaraman Purushothaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thippichettypalayam Ramasamy Gopala Krishna Murthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kuppannan Sukumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Palani Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vasudevan Gowthaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mohan Balusamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Robert Atterbury
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Suresh V. Kuchipudi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sellappan Saravanan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saravanan, S., Purushothaman, V., Murthy, T.R.G.K. et al. Molecular Epidemiology of Nontyphoidal Salmonella in Poultry and Poultry Products in India: Implications for Human Health. Indian J Microbiol 55, 319–326 (2015). https://doi.org/10.1007/s12088-015-0530-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-015-0530-z

Keywords

Search

Navigation