1887

Abstract

This study aimed to examine occurrence and antimicrobial resistance characteristics of from pigs, pork and humans in Thailand and Laos provinces. The samples were collected from pigs, carcasses and workers in slaughterhouses, retail pork and butchers in fresh markets and patients in hospitals in Thailand (=729) and Laos (=458). A total of 295 of 729 samples (34.6 %) collected in Thailand and 253 of 458 (47.4 %) samples collected in Laos were positive for . A total of 548 isolates from Thailand (=295) and Laos (=253) were further analysed. Serovar Typhimurium was the most common serotype in Thai (34 %) and Laos (20.6 %) samples. Approximately 2.4 % of Thai isolates produced extended-spectrum β-lactamase (ESBL). All the ESBL producers possessed , some of which were horizontally transferred. Class 1 integrons were common in Thai (31.9 %) and Laos (39.1 %) isolates, but none were associated with SGI1. The resistance cassette was the most common, while the least common was (=1). The gene cassette in five isolates and were located on conjugative plasmid. Three pork isolates were fluoroquinolone resistant and carried an amino acid substitute, Ser-83-Tyr, in GyrA. The gene was found in 7.1 and 5.5 % of the Thai and Laos isolates, respectively, while was carried in another Laos isolate (1.9 %). All ESBL producers carried In conclusion, multidrug-resistant was common in pigs, pork and human samples in this region. The bacteria carried mobile genetic elements and resistance genes on conjugative plasmids that could be readily transferred to other bacterial species.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000339
2016-10-18
2020-04-02
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/10/1182.html?itemId=/content/journal/jmm/10.1099/jmm.0.000339&mimeType=html&fmt=ahah

References

  1. ACSF 2006; Thai Agricultural Standard TAS 9009-2006. Good Manufacturing for Pig Abattoir pp.1–24 Bangkok, Thailand: National Bureau of Agricultural Commodity and Food Standards, Ministry of Agriculture and Cooperatives;
    [Google Scholar]
  2. ACSF 2010; Thai Agricultural Standard TAS 9034-2010. Good Practices for Animal Welfare: Manufacturing for Pig Abattoir pp.1–24 Bangkok, Thailand: National Bureau of Agricultural Commodity and Food Standards, Ministry of Agriculture and Cooperatives;
    [Google Scholar]
  3. Angkititrakul S., Chomvarin C., Chaita T., Kanistanon K., Waethewutajarn S.. 2005; Epidemiology of antimicrobial resistance in Salmonella isolated from pork, chicken meat and humans in Thailand. Southeast Asian J Trop Med Public Health36:1510–1515[PubMed]
    [Google Scholar]
  4. Asai T., Sato C., Masani K., Usui M., Ozawa M., Ogino T., Aoki H., Sawada T., Izumiya H. et al. 2010; Epidemiology of plasmid-mediated quinolone resistance in Salmonella enterica serovar typhimurium isolates from food-producing animals in Japan. Gut Pathog2:17 [CrossRef][PubMed]
    [Google Scholar]
  5. Bastiaensen P., Kamakawa A., Varas M.. 2011; OIE - PVS Evaluation Report of the Veterinary Services of the LAO People' DEmocratic Republic pp.1–180 Paris, France: World Organisation for Animal Health;
    [Google Scholar]
  6. Batchelor M., Hopkins K., Threlfall E. J., Clifton-Hadley F. A., Stallwood A. D., Davies R. H., Liebana E.. 2005; bla(CTX-M) genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother49:1319–1322 [CrossRef][PubMed]
    [Google Scholar]
  7. Bonnet R.. 2004; Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother48:1–14 [CrossRef][PubMed]
    [Google Scholar]
  8. Boonmar S., Markvichitr K., Chaunchom S., Chanda C., Bangtrakulnonth A., Pornrunangwong S., Yamamoto S., Suzuki D., Kozawa K. et al. 2008; Salmonella prevalence in slaughtered buffaloes and pigs and antimicrobial susceptibility of isolates in Vientiane, Lao People's Democratic Republic. J Vet Med Sci70:1345–1348 [CrossRef][PubMed]
    [Google Scholar]
  9. Boonmar S., Morita Y., Pulsrikarn C., Chaichana P., Pornruagwong S., Chaunchom S., Sychanh T., Khounsy T., Sisavath D. et al. 2013; Salmonella prevalence in meat at retail markets in Pakse, Champasak Province, Laos, and antimicrobial susceptibility of isolates. J Glob Antimicrob Resist1:157–161 [CrossRef]
    [Google Scholar]
  10. Cattoir V., Weill F. X., Poirel L., Fabre L., Soussy C. J., Nordmann P.. 2007; Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother59:751–754 [CrossRef][PubMed]
    [Google Scholar]
  11. Chen S., Zhao S., White D. G., Schroeder C. M., Lu R., Yang H., McDermott P. F., Ayers S., Meng J.. 2004; Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol70:1–7 [CrossRef][PubMed]
    [Google Scholar]
  12. Chiu C. H., Ou J. T.. 1996; 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. J Clin Microbiol34:2619–2622[PubMed]
    [Google Scholar]
  13. Chuanchuen R., Padungtod P.. 2009; Antibiotic resistance genes in Salmonella enterica isolates from poultry and swine. J Vet Med Sci70:1349–1355[CrossRef]
    [Google Scholar]
  14. Chuanchuen R., Khemtong S., Padungtod P.. 2007; Occurrence of qacE/qacEDelta1 genes and their correlation with class 1 integrons in S almonella enterica isolates from poultry and swine. Southeast Asian J Trop Med Public Health38:855–862[PubMed]
    [Google Scholar]
  15. CLSI 2013; Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  16. Cocks P., Abila R., Bouchot A., Benigno C., Morzaria S., Inthavong P., Long N. V., Luthi N. V., Scoizet A. et al. 2009; FAO ADB and OIE SEAFMD study on cross border movement and market chains of large ruminants and pigs in the Greater Mekong SubRegion.
  17. Crémet L., Caroff N., Dauvergne S., Reynaud A., Lepelletier D., Corvec S.. 2011; Prevalence of plasmid-mediated quinolone resistance determinants in ESBL Enterobacteriaceae clinical isolates over a 1-year period in a French hospital. Pathol Biol59:151–156 [CrossRef][PubMed]
    [Google Scholar]
  18. Doublet B., Lailler R., Meunier D., Brisabois A., Boyd D., Mulvey M. R., Chaslus-Dancla E., Cloeckaert A.. 2003; Variant Salmonella genomic island 1 antibiotic resistance gene cluster in Salmonella enterica serovar Albany. Emerg Infect Dis9:585–591 [CrossRef][PubMed]
    [Google Scholar]
  19. EFSA 2012; The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J10:2597–3039[CrossRef]
    [Google Scholar]
  20. Ekkapobyotin C., Padungtod P., Chuanchuen R.. 2008; Antimicrobial resistance of Campylobacter coli isolates from swine. Int J Food Microbiol128:325–328 [CrossRef][PubMed]
    [Google Scholar]
  21. Falvey L.. 2000; Thai Agriculture: Golden Cradle of Millennia Bangkok, Thailand: Kasetsart University Press;
    [Google Scholar]
  22. Ferrari R., Galiana A., Cremades R., Rodríguez J. C., Magnani M., Tognim M. C., Oliveira T. C., Royo G.. 2013; Plasmid-mediated quinolone resistance (PMQR) and mutations in the topoisomerase genes of Salmonella enterica strains from Brazil. Braz J Microbiol44:651–656 [CrossRef][PubMed]
    [Google Scholar]
  23. Gebreyes W. A., Thakur S., Davies P. R., Funk J. A., Altier C.. 2004; Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997-2000. J Antimicrob Chemother53:997–1003 [CrossRef][PubMed]
    [Google Scholar]
  24. Guerra B., Soto S., Helmuth R., Mendoza M. C.. 2002; Characterization of a self-transferable plasmid from Salmonella enterica serotype typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob Agents Chemother46:2977–2981 [CrossRef][PubMed]
    [Google Scholar]
  25. Hasman H., Mevius D., Veldman K., Olesen I., Aarestrup F. M.. 2005; Beta-lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother56:115–121 [CrossRef][PubMed]
    [Google Scholar]
  26. Hopkins K. L., Day M., Threlfall E. J.. 2008; Plasmid-mediated quinolone resistance in Salmonella enterica, United Kingdom. Emerg Infect Dis14:340–342 [CrossRef][PubMed]
    [Google Scholar]
  27. Hsu S. C., Chiu T. H., Pang J. C., Hsuan-Yuan C. H., Chang G. N., Tsen H. Y.. 2006; Characterisation of antimicrobial resistance patterns and class 1 integrons among Escherichia coli and Salmonella enterica serovar Choleraesuis strains isolated from humans and swine in Taiwan. Int J Antimicrob Agents27:383–391 [CrossRef][PubMed]
    [Google Scholar]
  28. ISO 2002; Microbiology of Food and Animal Feeding Stuffs – Horizontal Method for the Detection of Salmonella Spp: ISO6579-Fourth Edition Geneva, Switzerl: International Organization for Standardization;
    [Google Scholar]
  29. Izumiya H., Mori K., Higashide M., Tamura K., Takai N., Hirose K., Terajima J., Watanabe H.. 2005; Identification of CTX-M-14 {beta}-lactamase in a Salmonella enterica serovar enteritidis isolate from Japan. Antimicrob Agents Chemother49:2568–2570 [CrossRef][PubMed]
    [Google Scholar]
  30. Jin Y., Ling J. M.. 2006; CTX-M-producing Salmonella spp. in Hong Kong: an emerging problem. J Med Microbiol55:1245–1250 [CrossRef][PubMed]
    [Google Scholar]
  31. Jure M. A., Aulet O., Trejo A., Castillo M.. 2010; Extended-spectrum beta-lactamase-producing Salmonella enterica serovar Oranienburg (CTX-M-2 group) in a pediatric hospital in Tucumán, Argentina. Rev Soc Bras Med Trop43:121–124 [CrossRef][PubMed]
    [Google Scholar]
  32. Juttupornpong S., Choa-u-tai W., Tubcharoen S., Chaunchom S.. 1996; Survey on Status of Quality and Contaminations of Feed stuffs pp.1–22 Bangkok: Research and Development Institute, Kasetsart University;
    [Google Scholar]
  33. Kaferstein F. K., Motarjemi Y., Bettcher D. W.. 1997; Foodborne disease control: a transnational challenge. Emerg Infect Dis 3:503–510 [CrossRef][PubMed]
    [Google Scholar]
  34. Kameyama M., Chuma T., Yokoi T., Yabata J., Tominaga K., Miyasako D., Iwata H., Okamoto K.. 2012; Emergence of Salmonella enterica serovar infantis harboring IncI1 plasmid with bla(CTX-M-14) in a broiler farm in Japan. J Vet Med Sci74:1213–1216 [CrossRef][PubMed]
    [Google Scholar]
  35. Khemtong S., Chuanchuen R.. 2008; Class 1 integrons and Salmonella genomic island 1 among Salmonella enterica isolated from poultry and swine. Microb Drug Resist14:65–70 [CrossRef][PubMed]
    [Google Scholar]
  36. Kim K. Y., Park J. H., Kwak H. S., Woo G. J.. 2011; Characterization of the quinolone resistance mechanism in foodborne Salmonella isolates with high nalidixic acid resistance. Int J Food Microbiol146:52–56 [CrossRef][PubMed]
    [Google Scholar]
  37. Knips V.. 2004; Review of the Livestock Sector in the Mekong Countries Food and Agriculture Organization of the United Nations;
    [Google Scholar]
  38. Lévesque C., Piché L., Larose C., Roy P. H.. 1995; PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother39:185–191 [CrossRef][PubMed]
    [Google Scholar]
  39. Levings R. S., Hall R. M., Lightfoot D., Djordjevic S. P.. 2006; linG, a new integron-associated gene cassette encoding a lincosamide nucleotidyltransferase. Antimicrob Agents Chemother50:3514–3515 [CrossRef][PubMed]
    [Google Scholar]
  40. Li R., Lai J., Wang Y., Liu S., Li Y., Liu K., Shen J., Wu C.. 2013; Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China. Int J Food Microbiol163:14–18 [CrossRef][PubMed]
    [Google Scholar]
  41. Majowicz S. E., Musto J., Scallan E., Angulo F. J., Kirk M., O'Brien S. J., Jones T. F., Fazil A., Hoekstra R. M.. International Collaboration on Enteric Disease ‘Burden of Illness' Studies 2010; The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis50:882–889 [CrossRef][PubMed]
    [Google Scholar]
  42. Makendi C., Page A. J., Wren B. W., Le Thi Phuong T., Clare S., Hale C., Goulding D., Klemm E. J., Pickard D. et al. 2016; A phylogenetic and phenotypic analysis of Salmonella enterica serovar Weltevreden, an emerging agent of diarrheal disease in tropical regions. PLoS Negl Trop Dis10:e0004446 [CrossRef][PubMed]
    [Google Scholar]
  43. Padungtod P., Kaneene J. B.. 2006; Salmonella in food animals and humans in northern Thailand. Int J Food Microbiol108:346–354 [CrossRef][PubMed]
    [Google Scholar]
  44. Paitoonpong S.. 2006; Thailand’s cross-border trade in the Greater Mekong Subregion: some issues never solved. TDRI Quaterly Review21:11–19
    [Google Scholar]
  45. Park C. H., Robicsek A., Jacoby G. A., Sahm D., Hooper D. C.. 2006; Prevalence in the United States of aac(6')-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother50:3953–3955 [CrossRef][PubMed]
    [Google Scholar]
  46. Partridge S. R., Tsafnat G., Coiera E., Iredell J. R.. 2009; Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev33:757–784 [CrossRef][PubMed]
    [Google Scholar]
  47. Paterson D. L.. 2000; Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs). Clin Microbiol Infect6:460–463 [CrossRef][PubMed]
    [Google Scholar]
  48. Pitout J. D., Hossain A., Hanson N. D.. 2004; Phenotypic and molecular detection of CTX-M-beta-lactamases produced by Escherichia coli and Klebsiella spp. J Clin Microbiol42:5715–5721 [CrossRef][PubMed]
    [Google Scholar]
  49. Polly C., Ronello A., Alexandre B., Carolyn B., Subhash M., Pouth I., Nguyen V. L., Nancy B. L., Axelle S. et al. 2009; FAOADB and OIE SEAFMD Study on CrossBorder Movement and Marketchains of Large Ruminants and Pigs in the Greater Mekong SubRegion pp.1–63 Bangkok, Thailand:
    [Google Scholar]
  50. Popoff M., LeMinor L.. 1992; Antigenic formulas of the Salmonellla Serovars Paris: Institut Pasteur;
    [Google Scholar]
  51. Pulsrikarn C., Chaichana P., Pornruangwong S., Morita Y., Yamamoto S., Boonmar S.. 2012; Serotype, antimicrobial susceptibility, and genotype of Salmonella isolates from swine and pork. Thai J Vet Med 42:21–27
    [Google Scholar]
  52. Senok A. C., Botta G. A., Soge O. O.. 2012; Emergence and spread of antimicrobial-resistant pathogens in an era of globalization. Interdiscip Perspect Infect Dis2012:1–3
    [Google Scholar]
  53. Sinwat N., Angkittitrakul S., Chuanchuen R.. 2015; Characterizationof antimicrobial resistance in Salmonella enterica isolated from pork, chickenmeat and humans in Northeastern Thailand. Foodborne Pathog Dis12:759–765 [CrossRef][PubMed]
    [Google Scholar]
  54. Skyberg J. A., Logue C. M., Nolan L. K.. 2006; Virulence genotyping of Salmonella spp. with multiplex PCR. Avian Dis50:77–81 [CrossRef][PubMed]
    [Google Scholar]
  55. Stephenson S., Brown P. D., Holness A., Wilks M.. 2010; The emergence of qnr-mediated quinolone resistance among Enterobacteriaceae in Jamaica. West Indian Med J59:241–244[PubMed]
    [Google Scholar]
  56. Sunde M.. 2005; Prevalence and characterization of class 1 and class 2 integrons in Escherichia coli isolated from meat and meat products of Norwegian origin. J Antimicrob Chemother56:1019–1024 [CrossRef][PubMed]
    [Google Scholar]
  57. Thai T. H., Yamaguchi R.. 2012; Molecular characterization of antibiotic-resistant Salmonella isolates from retail meat from markets in Northern Vietnam. J Food Prot75:1709–1714 [CrossRef][PubMed]
    [Google Scholar]
  58. Thai T. H., Hirai T., Lan N. T., Yamaguchi R.. 2012; Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol156:147–151 [CrossRef][PubMed]
    [Google Scholar]
  59. Warburg G., Korem M., Robicsek A., Engelstein D., Moses A. E., Block C., Strahilevitz J.. 2009; Changes in aac(6')-Ib-cr prevalence and fluoroquinolone resistance in nosocomial isolates of Escherichia coli collected from 1991 through 2005. Antimicrob Agents Chemother53:1268–1270 [CrossRef][PubMed]
    [Google Scholar]
  60. WHO 2015; Global Action Plan on Antimicrobial Resistance Geneva, Switzerland: WHO Document Service;
    [Google Scholar]
  61. Wong M. H., Chan E. W., Liu L. Z., Chen S.. 2014a; PMQR genes oqxAB and aac(6')Ib-cr accelerate the development of fluoroquinolone resistance in Salmonella typhimurium. Front Microbiol5:521 [CrossRef][PubMed]
    [Google Scholar]
  62. Wong M. H., Yan M., Chan E. W., Biao K., Chen S.. 2014b; Emergence of clinical Salmonella enterica serovar Typhimurium isolates with concurrent resistance to ciprofloxacin, ceftriaxone, and azithromycin. Antimicrob Agents Chemother58:3752–3756 [CrossRef][PubMed]
    [Google Scholar]
  63. Wu J. J., Ko W. C., Wu H. M., Yan J. J.. 2008; Prevalence of Qnr determinants among bloodstream isolates of Escherichia coli and Klebsiella pneumoniae in a Taiwanese hospital, 1999–2005. J Antimicrob Chemother61:1234–1239 [CrossRef][PubMed]
    [Google Scholar]
  64. Yamane K., Wachino J., Suzuki S., Arakawa Y.. 2008; Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother52:1564–1566 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000339
Loading
/content/journal/jmm/10.1099/jmm.0.000339
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error