Skip to main content Accessibility help
×
Home

High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam

  • L. T. P. TU (a1), N. V. M. HOANG (a1), N. V. CUONG (a1), J. CAMPBELL (a1) (a2), J. E. BRYANT (a1) (a2), N. T. HOA (a1) (a2), B. T. KIET (a3), C. THOMPSON (a1), D. T. DUY (a1), V. V. PHAT (a1), V. B. HIEN (a3), G. THWAITES (a1) (a2), S. BAKER (a1) (a2) (a4) and J. J. CARRIQUE-MAS (a1) (a2)...

Summary

We investigated the prevalence, diversity, and antimicrobial resistance (AMR) profiles of non-typhoidal Salmonella (NTS) and associated risk factors on 341 pig, chicken, and duck farms in Dong Thap province (Mekong Delta, Vietnam). Sampling was stratified by species, district (four categories), and farm size (three categories). Pooled faeces, collected using boot swabs, were tested using ISO 6575: 2002 (Annex D). Isolates were serogrouped; group B isolates were tested by polymerase chain reaction to detect S. Typhimurium and (monophasic) serovar 4,[5],12:i:- variants. The farm-level adjusted NTS prevalence was 64·7%, 94·3% and 91·3% for chicken, duck and pig farms, respectively. Factors independently associated with NTS were duck farms [odds ratio (OR) 21·2], farm with >50 pigs (OR 11·9), pig farm with 5–50 pigs (OR 4·88) (vs. chickens), and frequent rodent sightings (OR 2·3). Both S. Typhimurium and monophasic S. Typhimurium were more common in duck farms. Isolates had a high prevalence of resistance (77·6%) against tetracycline, moderate resistance (20–30%) against chloramphenicol, sulfamethoxazole-trimethoprim, ampicillin and nalidixic acid, and low resistance (<5%) against ciprofloxacin and third-generation cephalosporins. Multidrug resistance (resistance against ⩾3 classes of antimicrobial) was independently associated with monophasic S. Typhimurium and other group B isolates (excluding S. Typhimurium) and pig farms. The unusually high prevalence of NTS on Mekong Delta farms poses formidable challenges for control.

  • 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.

      High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam
      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.

      High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam
      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.

      High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

* Author for correspondence: Dr J. J Carrique-Mas, Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 764, Vo Van Kiet, Ho Chi Minh City, Vietnam. (Email: jcarrique-mas@oucru.org)

References

Hide All
1. Pegues, D, Miller, SI. Salmonella species, including Salmonella Typhi. In: Mandell, G, Bennet, J, Dolin, R, eds. Principle and Practice of Infectious Diseases. Philadelphia: Churchill Livingstone Elsevier, 2010, pp. 28872903.
2. Carrique-Mas, JJ, Bryant, JE. A review of foodborne bacterial and parasitic zoonoses in Vietnam. Ecohealth 2013; 10: 465489.
3. Nga, TV, et al. The decline of typhoid and the rise of non-typhoid salmonellae and fungal infections in a changing HIV landscape: bloodstream infection trends over 15 years in southern Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene 2012; 106: 2634.
4. Thompson, CN, et al. Epidemiological features and risk factors of Salmonella gastroenteritis in children resident in Ho Chi Minh City, Vietnam. Epidemiology and Infection 2012; 141: 110.
5. Vo, ATT, et al. Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella Typhimurium phage type 90. Veterinary Microbiology 2006; 113: 153158.
6. Switt, AI, et al. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i. Foodborne Pathogens and Disease 2009; 6: 407415.
7. Phan, TT, et al. Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, Vietnam. Journal of Food Protection 2005; 68: 10771080.
8. Van, TT, et al. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Applied and Environmental Microbiology 2007; 73: 68856890.
9. Thai, TH, et al. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. International Journal of Food Microbiology 2012; 156: 147151.
10. Ta, YT, et al. Prevalence of Salmonella on chicken carcasses from retail markets in Vietnam. Journal of Food Protection 2012; 75: 18511854.
11. Thai, TH, Yamaguchi, R. Molecular characterization of antibiotic-resistant Salmonella isolates from retail meat from markets in Northern Vietnam. Journal of Food Protection 2012; 75: 17091714.
12. Ta, YT, et al. Quantification, serovars, and antibiotic resistance of salmonella isolated from retail raw chicken meat in Vietnam. Journal of Food Protection 2014; 77: 5766.
13. Carrique-Mas, JJ, et al. An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiology and Infection 2013; 142: 14251436.
14. Arnold, ME, Cook, AJ. Estimation of sample sizes for pooled faecal sampling for detection of Salmonella in pigs. Epidemiology and Infection 2009; 137: 17341741.
15. Arnold, ME, et al. A comparison of pooled and individual bird sampling for detection of Salmonella in commercial egg laying flocks. Preventive Veterinary Medicine 2011; 99: 176184.
16. Carrique-Mas, JJ, Davies, RH. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: a review. Revue Scientifique et Technique (International Office of Epizootics) 2008; 27: 665677.
17. Skov, MN, et al. Evaluation of sampling methods for the detection of Salmonella in broiler flocks. Journal of Applied Microbiology 1999; 86: 695700.
18. Arnold, ME, et al. Estimation of the sensitivity of environmental sampling for detection of Salmonella in commercial layer flocks post-introduction of national control programmes. Epidemiology and Infection 2014; 142: 10611069.
19. Carrique-Mas, JJ, et al. Comparison of three plating media for the isolation of Salmonella from poultry environmental samples in Great Britain using ISO 6579:2002 (Annex D). Journal of Applied Microbiology 2009; 107: 19761983.
20.Anon. Antigenic Formulae of the Salmonella Serovars. 9th edn. WHO Collaborating Center for Reference and Research on Salmonella, 2007.
21. Tennant, SM, et al. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Neglected Tropical Diseases 2010; 4: e621.
22. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing, Twenty-First Informational Supplement, 2011, 100-S21, vol. 31, no. 1, pp. 42–58.
23. Dohoo, I, Martyn, W, Stryhn, H. Veterinary Epidemiologic Research. Charlottetown, Canada: AVC Inc., 2003.
24. Hosmer, D, Lemeshow, S. 2000. Applied Logistic Regression, 2nd edn. John Wiley and Sons, Hoboken, USA.
25. EFSA. Analysis of the baseline survey on the prevalence of Salmonella in holdings with breeding pigs in the EU, 2008: Part A: Salmonella prevalence estimates. EFSA Journal 2009; 7: 1377.
26. EFSA. Report of the Task Force on Zoonoses Data Collection on the Analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus, in the EU, 2005–2006. EFSA Journal 2007; 98: 185.
27. 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.
28. Minh, PQ, et al. A description of the management of itinerant grazing ducks in the Mekong river delta of Vietnam. Preventive Veterinary Medicine 2010; 94: 101107.
29. Tran, TP, et al. Prevalence of Salmonella spp. in pigs, chickens and ducks in the Mekong Delta, Vietnam. Journal of Veterinary Medical Science 2004; 66: 10111014.
30. EFSA. The European Union Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA Journal 2014; 12 (2): 3547 (312pp).
31. Arnold, ME, Carrique-Mas, JJ, Davies, RH. Sensitivity of environmental sampling methods for detecting Salmonella Enteritidis in commercial laying flocks relative to the within-flock prevalence. Epidemiology and Infection 2010; 138: 330339.
32. Carrique-Mas, JJ, et al. Persistence and clearance of different Salmonella serovars in buildings housing laying hens. Epidemiology and Infection 2009; 137: 837846.
33. Davies, RH, Wray, C. Mice as carriers of Salmonella enteritidis on persistently infected poultry units. Veterinary Record 1995; 137: 337341.
34. Phan, TT, et al. Prevalence of Salmonella spp. in rice-field rats in the Mekong delta, Vietnam. Journal of Veterinary Epidemiology 2005; 9: 8588.
35. Beloeil, PA, et al. Risk factors for Salmonella seroconversion of fattening pigs in farrow-to-finish herds. Veterinary Research 2007; 38: 835848.
36. Garcia-Feliz, C, et al. Herd-level risk factors for faecal shedding of Salmonella enterica in Spanish fattening pigs. Preventive Veterinary Medicine 2009; 91: 130136.
37. Wray, C. Salmonella in Domestic Animals. Oxon, UK: CABI Publishing, 2000.
38. Bergeron, N, et al. Characterization of Salmonella Typhimurium isolates associated with septicemia in swine. Canadian Journal of Veterinary Research 2010; 74: 1117.
39. Wagenaar, JA, Hendriksen, RS, Carrique-Mas, J. Practical considerations of surveillance of Salmonella serovars other than Enteritidis and Typhimurium. Revue Scientifique et Technique (International Office of Epizootics) 2013; 32: 509519.
40. Hauser, E, et al. Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Applied and Environmental Microbiology 2010; 76: 46014610.
41. Ha Thai, T, Yamaguchi, R. Molecular characterization of antibiotic-resistant salmonella isolates from retail meat from markets in northern Vietnam. Journal of Food Protection 2012; 75: 17091714.
42. EFSA. The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010. EFSA Journal 2012; 10: 233.
43. Vo, ATT, et al. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS ONE 2010; 5: e9440.
44. Van, TT, et al. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. International Journal of Food Microbiology 2012; 154: 98106.
45. Hopkins, KL, et al. Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: a new pandemic strain? Eurosurveillance 2010; 15: pii = 19 580.
46. Deng, X, et al. Laboratory-based surveillance of non-typhoidal Salmonella infections in Guangdong Province, China. Foodborne Pathogens and Disease 2012; 9: 305312.

Keywords

Type Description Title
WORD
Supplementary materials

Tu supplementary material
Table S1

 Word (14 KB)
14 KB

Metrics

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