1887

Abstract

spp. are a leading cause of bacterial foodborne zoonosis worldwide, with poultry meat and products recognised as a significant source of human infection. In Vietnam there are few data regarding the occurrence, antimicrobial resistance, and genomic diversity of in poultry and poultry meat. The aim of this study was to estimate the prevalence of in chicken meat at retail in Hanoi, determine antimicrobial sensitivities of the isolated, and assess their genetic diversity. A total of 120 chicken meat samples were collected from eight traditional retail markets (=80) and four supermarkets (=40). was isolated following ISO 10272-1 : 2017 and identification verified by PCR. The prevalence of was 38.3 % (46/120) and was the most prevalent species in both retail markets (74 %) and supermarkets (88 %). The minimum inhibitory concentrations for ciprofloxacin, erythromycin, gentamicin, nalidixic acid, streptomycin, and tetracycline were determined by broth microdilution for 32 isolates. All characterised were resistant to ciprofloxacin, nalidixic acid, and tetracycline, with corresponding resistance determinants detected in the sequenced genomes. Most were multidrug resistant (24/28) and two harboured the erythromycin resistance gene on a multiple drug-resistance genomic island, a potential mechanism for dissemination of resistance. The 32 isolates belonged to clonal complexes associated with both poultry and people, such as CC828 for . These results contribute to the One Health approach for addressing in Vietnam by providing detailed new insights into a main source of human infection and can inform the design of future surveillance approaches.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001190
2024-01-31
2024-11-07
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/1/mgen001190.html?itemId=/content/journal/mgen/10.1099/mgen.0.001190&mimeType=html&fmt=ahah

References

  1. CDC Campylobacter [Online]; 2019 https://www.cdc.gov/campylobacter/faq.html
  2. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2012. EFS2 2014; 12:3547 [View Article]
    [Google Scholar]
  3. Ruiz-Palacios GM. The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clin Infect Dis 2007; 44:701–703 [View Article] [PubMed]
    [Google Scholar]
  4. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 2015; 12:e1001923 [View Article] [PubMed]
    [Google Scholar]
  5. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015; 28:687–720 [View Article] [PubMed]
    [Google Scholar]
  6. Sahin O, Zhang Q, Meitzler JC, Harr BS, Morishita TY et al. Prevalence, antigenic specificity, and bactericidal activity of poultry anti-Campylobacter maternal antibodies. Appl Environ Microbiol 2001; 67:3951–3957 [View Article] [PubMed]
    [Google Scholar]
  7. Lamb-Rosteski JM, Kalischuk LD, Inglis GD, Buret AG. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect Immun 2008; 76:3390–3398 [View Article] [PubMed]
    [Google Scholar]
  8. El-Aziz DMA, Abd-Allah SM. Incidence of Campylobacter species in wholesale chicken carcasses and chicken meat products in Assiut city. Egypt Int Food Res J 2017; 24:2660–2665
    [Google Scholar]
  9. Wagenaar JA, French NP, Havelaar AH. Preventing Campylobacter at the source: why is it so difficult?. Clin Infect Dis 2013; 57:1600–1606 [View Article] [PubMed]
    [Google Scholar]
  10. European Food Safety Authority (EFSA)European Centre for Disease Prevention and Control (ECDC) The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021. EFSA J 2023; 21:e07867 [View Article] [PubMed]
    [Google Scholar]
  11. Luangtongkum T, Jeon B, Han J, Plummer P, Logue CM et al. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol 2009; 4:189–200 [View Article] [PubMed]
    [Google Scholar]
  12. Nguyen NH, Nguyen TNM, Hotzel H, El Adawy H, Nguyen AQ et al. Thermophilic Campylobacter - neglected foodborne pathogens in Cambodia, Laos and Vietnam. Gastroenterol Hepatol 2017; 8:00279 [View Article] [PubMed]
    [Google Scholar]
  13. Anders KL, Thompson CN, Thuy NTV, Nguyet NM, Tu LTP et al. The epidemiology and aetiology of diarrhoeal disease in infancy in southern Vietnam: a birth cohort study. Int J Infect Dis 2015; 35:3–10 [View Article] [PubMed]
    [Google Scholar]
  14. Bodhidatta L, Lan NTP, Hien BT, Lai NV, Srijan A et al. Rotavirus disease in young children from Hanoi, Vietnam. Pediatr Infect Dis J 2007; 26:325–328 [View Article] [PubMed]
    [Google Scholar]
  15. Thompson CN, Phan MVT, Hoang NVM, Minh PV, Vinh NT et al. A prospective multi-center observational study of children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. Am J Trop Med Hyg 2015; 92:1045–1052 [View Article] [PubMed]
    [Google Scholar]
  16. Thi Dien N, Thi Minh Khue N, Ebata A, Fournié G, Huyen LTT et al. Mapping chicken production and distribution networks in Vietnam: an analysis of socio-economic factors and their epidemiological significances. Prev Vet Med 2023; 214:105906 [View Article] [PubMed]
    [Google Scholar]
  17. Minh VD, Meeyam T, Unger F, Gölz G, Ngoc PT et al. Prevalence of Campylobacter spp. on retail fresh chicken carcasses in Hanoi, Vietnam. VIS 2023; 21:221–227 [View Article]
    [Google Scholar]
  18. Carrique-Mas JJ, Bryant JE, Cuong NV, Hoang NVM, Campbell J et al. An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiol Infect 2014; 142:1425–1436 [View Article] [PubMed]
    [Google Scholar]
  19. Schwan P. Prevalence and Antibiotic Resistance of Campylobacter Spp. in Poultry and Raw Meat in the Can Tho Province, Vietnam Swedish University of Agricultural Sciences; 2010
    [Google Scholar]
  20. Ha TAD, Pham TY. Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, Vietnam. Ann N Y Acad Sci 2006; 1081:262–265 [View Article] [PubMed]
    [Google Scholar]
  21. Garin B, Gouali M, Wouafo M, Perchec A-M, Pham MT et al. Prevalence, quantification and antimicrobial resistance of Campylobacter spp. on chicken neck-skins at points of slaughter in 5 major cities located on 4 continents. Int J Food Microbiol 2012; 157:102–107 [View Article] [PubMed]
    [Google Scholar]
  22. Luu QH, Tran TH, Phung DC, Nguyen TB. Study on the prevalence of Campylobacter spp. from chicken meat in Hanoi, Vietnam. Ann N Y Acad Sci 2006; 1081:273–275 [View Article] [PubMed]
    [Google Scholar]
  23. Nguyen TNM, Hotzel H, El-Adawy H, Tran HT, Le MTH et al. Genotyping and antibiotic resistance of thermophilic Campylobacter isolated from chicken and pig meat in Vietnam. Gut Pathog 2016; 8:19 [View Article] [PubMed]
    [Google Scholar]
  24. Cody AJ, Maiden MC, Strachan NJ, McCarthy ND. A systematic review of source attribution of human campylobacteriosis using multilocus sequence typing. Euro Surveill 2019; 24:1800696 [View Article] [PubMed]
    [Google Scholar]
  25. Arning N, Sheppard SK, Bayliss S, Clifton DA, Wilson DJ. Machine learning to predict the source of campylobacteriosis using whole genome data. PLoS Genet 2021; 17:e1009436 [View Article] [PubMed]
    [Google Scholar]
  26. Petrie A, Watson PF. Statistics for Veterinary and Animal Science. Third edition ed Chichester, West Sussex: Wiley-Blackwell, a John Wiley Sons, Ltd., publication Chichester, West Sussex; 2013
    [Google Scholar]
  27. Schwarz S, Silley P, Simjee S, Woodford N, van Duijkeren E et al. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Vet Microbiol 2010; 141:1–4 [View Article] [PubMed]
    [Google Scholar]
  28. Seemann T, Bulach DM, Schultz MB, Kwong JC, Howden BP. Nullarbor Github; 2020
    [Google Scholar]
  29. Pearson BM, Rokney A, Crossman LC, Miller WG, Wain J et al. Complete genome sequence of the Campylobacter coli clinical isolate 15-537360. Genome Announc 2013; 1:e01056-13 [View Article] [PubMed]
    [Google Scholar]
  30. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  32. Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother 2019; 63:e00483-19 [View Article] [PubMed]
    [Google Scholar]
  33. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  34. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  35. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–5 [View Article] [PubMed]
    [Google Scholar]
  36. Lay KS, Vuthy Y, Song P, Phol K, Sarthou JL. Prevalence, numbers and antimicrobial susceptibilities of Salmonella serovars and Campylobacter spp. in retail poultry in Phnom Penh, Cambodia. J Vet Med Sci 2011; 73:325–329 [View Article] [PubMed]
    [Google Scholar]
  37. Sallam KI. Prevalence of Campylobacter in chicken and chicken by-products retailed in Sapporo area, Hokkaido, Japan. Food Control 2007; 18:1113–1120 [View Article]
    [Google Scholar]
  38. Szosland-Fałtyn A, Bartodziejska B, Królasik J, Paziak-Domańska B, Korsak D et al. The prevalence of Campylobacter spp. in polish poultry meat. Pol J Microbiol 2018; 67:117–120 [View Article] [PubMed]
    [Google Scholar]
  39. Wong TL, Hudson JA. Campylobacter Spp. in Uncooked Retail Chicken Meats Ministry of Agriculture and Forestry; 2011
    [Google Scholar]
  40. Moran L, Scates P, Madden RH. Prevalence of Campylobacter spp. in raw retail poultry on sale in Northern Ireland. J Food Prot 2009; 72:1830–1835 [View Article] [PubMed]
    [Google Scholar]
  41. Nobile CGA, Costantino R, Bianco A, Pileggi C, Pavia M. Prevalence and pattern of antibiotic resistance of Campylobacter spp. in poultry meat in Southern Italy. Food Control 2013; 32:715–718 [View Article]
    [Google Scholar]
  42. Prencipe V, Parisciani G, Calistri P, Caporale CM, Iannitto G et al. Thermotolerant Campylobacter in poultry meat marketed in the Abruzzo and Molise regions of Italy: prevalence and contamination levels. Vet Ital 2007; 43:167–174 [PubMed]
    [Google Scholar]
  43. Sammarco ML, Ripabelli G, Fanelli I, Grasso GM, Tamburro M. Prevalence and biomolecular characterization of Campylobacter spp. isolated from retail meat. J Food Prot 2010; 73:720–728 [View Article] [PubMed]
    [Google Scholar]
  44. Stella S, Soncini G, Ziino G, Panebianco A, Pedonese F et al. Prevalence and quantification of thermophilic Campylobacter spp. in Italian retail poultry meat: analysis of influencing factors. Food Microbiol 2017; 62:232–238 [View Article] [PubMed]
    [Google Scholar]
  45. Rouger A, Tresse O, Zagorec M. Bacterial contaminants of poultry meat: sources, species, and dynamics. Microorganisms 2017; 5:50 [View Article] [PubMed]
    [Google Scholar]
  46. Zhang P, Zhang X, Liu Y, Jiang J, Shen Z et al. Multilocus sequence types and antimicrobial resistance of Campylobacter jejuni and C. coli isolates of human patients from Beijing, China, 2017-2018. Front Microbiol 2020; 11:554784 [View Article] [PubMed]
    [Google Scholar]
  47. Dearlove BL, Cody AJ, Pascoe B, Méric G, Wilson DJ et al. Rapid host switching in generalist Campylobacter strains erodes the signal for tracing human infections. ISME J 2016; 10:721–729 [View Article] [PubMed]
    [Google Scholar]
  48. Cody AJ, McCarthy NM, Wimalarathna HL, Colles FM, Clark L et al. A longitudinal 6-year study of the molecular epidemiology of clinical campylobacter isolates in Oxfordshire, United kingdom. J Clin Microbiol 2012; 50:3193–3201 [View Article] [PubMed]
    [Google Scholar]
  49. Cobo-Díaz JF, González del Río P, Álvarez-Ordóñez A. Whole resistome analysis in Campylobacter jejuni and C. coli genomes available in public repositories. Front Microbiol 2021; 12:662144 [View Article]
    [Google Scholar]
  50. Feodoroff B, de Haan CPA, Ellström P, Sarna S, Hänninen M-L et al. Clonal distribution and virulence of Campylobacter jejuni isolates in blood. Emerg Infect Dis 2013; 19:1653–1655 [View Article] [PubMed]
    [Google Scholar]
  51. Moffatt CRM, Greig A, Valcanis M, Gao W, Seemann T et al. A large outbreak of Campylobacter jejuni infection in a university college caused by chicken liver pâté, Australia, 2013. Epidemiol Infect 2016; 144:2971–2978 [View Article] [PubMed]
    [Google Scholar]
  52. Wysok B, Wojtacka J, Hänninen M-L, Kivistö R. Antimicrobial resistance and virulence-associated markers in Campylobacter strains from diarrheic and non-diarrheic humans in Poland. Front Microbiol 2020; 11:1799 [View Article] [PubMed]
    [Google Scholar]
  53. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA J 2020; 18:e06007 [View Article] [PubMed]
    [Google Scholar]
  54. Mourkas E, Florez-Cuadrado D, Pascoe B, Calland JK, Bayliss SC et al. Gene pool transmission of multidrug resistance among Campylobacter from livestock, sewage and human disease. Environ Microbiol 2019; 21:4597–4613 [View Article] [PubMed]
    [Google Scholar]
  55. Alfredson DA, Korolik V. Antibiotic resistance and resistance mechanisms in Campylobacter jejuni and Campylobacter coli. FEMS Microbiol Lett 2007; 277:123–132 [View Article] [PubMed]
    [Google Scholar]
  56. Hormeño L, Campos MJ, Vadillo S, Quesada A. Occurrence of tet(O/M/O) mosaic gene in tetracycline-resistant Campylobacter. Microorganisms 2020; 8:1710
    [Google Scholar]
  57. Yao H, Liu D, Wang Y, Zhang Q, Shen Z. High prevalence and predominance of the aph(2″)-If gene conferring aminoglycoside resistance in Campylobacter. Antimicrob Agents Chemother 2017; 61:e00112-17 [View Article] [PubMed]
    [Google Scholar]
  58. Qin S, Wang Y, Zhang Q, Chen X, Shen Z et al. Identification of a novel genomic island conferring resistance to multiple aminoglycoside antibiotics in Campylobacter coli. Antimicrob Agents Chemother 2012; 56:5332–5339 [View Article] [PubMed]
    [Google Scholar]
  59. Carrique-Mas JJ, Trung NV, Hoa NT, Mai HH, Thanh TH et al. Antimicrobial usage in chicken production in the Mekong Delta of Vietnam. Zoonoses Public Health 2015; 62 Suppl 1:70–78 [View Article] [PubMed]
    [Google Scholar]
  60. Zeitouni S, Collin O, Andraud M, Ermel G, Kempf I. Fitness of macrolide resistant Campylobacter coli and Campylobacter jejuni. Microb Drug Resist 2012; 18:101–108 [View Article] [PubMed]
    [Google Scholar]
  61. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  62. Bolinger H, Kathariou S. The current state of macrolide resistance in Campylobacter spp.: trends and impacts of resistance mechanisms. Appl Environ Microbiol 2017; 83:e00416-17 [View Article] [PubMed]
    [Google Scholar]
  63. Wallace RL, Bulach D, Valcanis M, Polkinghorne BG, Pingault N et al. Identification of the first erm(B)-positive Campylobacter jejuni and Campylobacter coli associated with novel multidrug resistance genomic islands in Australia. J Glob Antimicrob Resist 2020; 23:311–314 [View Article] [PubMed]
    [Google Scholar]
  64. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
  65. Qin S, Wang Y, Zhang Q, Zhang M, Deng F et al. Report of ribosomal RNA methylase gene erm(B) in multidrug-resistant Campylobacter coli. J Antimicrob Chemother 2014; 69:964–968 [View Article] [PubMed]
    [Google Scholar]
  66. Denis M, Soumet C, Rivoal K, Ermel G, Blivet D et al. Development of a m-PCR assay for simultaneous identification of Campylobacter jejuni and C. coli. Lett Appl Microbiol 1999; 29:406–410 [View Article] [PubMed]
    [Google Scholar]
  67. Cardarelli-Leite P, Blom K, Patton CM, Nicholson MA, Steigerwalt AG et al. Rapid identification of Campylobacter species by restriction fragment length polymorphism analysis of a PCR-amplified fragment of the gene coding for 16S rRNA. J Clin Microbiol 1996; 34:62–67 [View Article] [PubMed]
    [Google Scholar]
  68. Deng F, Wang Y, Zhang Y, Shen Z. Characterization of the genetic environment of the ribosomal RNA methylase gene erm(B) in Campylobacter jejuni. J Antimicrob Chemother 2015; 70:613–615 [View Article] [PubMed]
    [Google Scholar]
  69. Tang B, Wang Y, Luo Y, Zheng X, Qin X et al. Coexistence of optrA and fexA in Campylobacter. mSphere 2021; 6: [View Article]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001190
Loading
/content/journal/mgen/10.1099/mgen.0.001190
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL
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