1887

Abstract

Consumption of prawns as a protein source has been on the rise worldwide with seafood identified as the predominant attributable source of human vibriosis. However, surveillance of non-cholera is limited both in public health and in food. Using a population- and market share-weighted study design, 211 prawn samples were collected and cultured for spp. Contamination was detected in 46 % of samples, and multiple diverse isolates were obtained from 34 % of positive samples. Whole genome sequencing (WGS) and phylogenetic analysis illustrated a comprehensive view of species diversity in prawns available at retail, with no known pathogenicity markers identified in and . Antimicrobial resistance genes were found in 77 % of isolates, and 12 % carried genes conferring resistance to three or more drug classes. Resistance genes were found predominantly in , though multiple resistance genes were also identified in and . This study highlights the large diversity in derived from prawns at retail, even within a single sample. Although there was little evidence in this study that prawns are a major source of vibriosis in the UK, surveillance of non-cholera is very limited. This study illustrates the value of expanding WGS surveillance efforts of non-cholera Vibrios in the food chain to identify critical control points for food safety through the production system and to determine the full extent of the public health impact.

Funding
This study was supported by the:
  • food standards agency (Award FS101185)
    • Principle Award Recipient: AlisonMather
  • biotechnology and biological sciences research council (Award BBS/E/F/000PR10348)
    • Principle Award Recipient: AlisonMather
  • biotechnology and biological sciences research council (Award BB/R012504/1)
    • Principle Award Recipient: AlisonMather
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-09-29
2021-11-29
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References

  1. Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK et al. Vibrio spp. infections. Nat Rev Dis Primers 2018; 4:8 [View Article] [PubMed]
    [Google Scholar]
  2. Baker-Austin C, Jenkins C, Dadzie J, Mestanza O, Delgado E et al. Genomic epidemiology of domestic and travel-associated Vibrio parahaemolyticus infections in the UK, 2008–2018. Food Control 2020; 115: [View Article]
    [Google Scholar]
  3. 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]
    [Google Scholar]
  4. Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [View Article] [PubMed]
    [Google Scholar]
  5. Vu TTT, Alter T, Huehn S. Prevalence of Vibrio spp. in retail seafood in Berlin, Germany. J Food Prot 2018; 81:593–597 [View Article] [PubMed]
    [Google Scholar]
  6. Janda JM, Newton AE, Bopp CA. Vibriosis. Clin Lab Med 2015; 35:273–288 [View Article] [PubMed]
    [Google Scholar]
  7. Jones JL. Vibrio: Introduction, including Vibrio parahaemolyticus, Vibrio vulnificus, and other Vibrio species. Encyclopedia of Food Microbiology, Second Edition. Elsevier; 2014 pp 691–698
    [Google Scholar]
  8. Yen NTP, Nhung NT, NTB V, Cuong NV, Tien Chau LT et al. Antimicrobial residues, non-typhoidal Salmonella, Vibrio spp. and associated microbiological hazards in retail shrimps purchased in Ho Chi Minh City (Vietnam. Food Control 2020; 107:106756 [View Article] [PubMed]
    [Google Scholar]
  9. Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. Non-cholera Vibrios: the microbial barometer of climate change. Trends Microbiol 2017; 25:76–84 [View Article] [PubMed]
    [Google Scholar]
  10. Banerjee SK, Farber JM. Detection, enumeration, and isolation of Vibrio parahaemolyticus and V. vulnificus from seafood: development of a multidisciplinary protocol. J AOAC Int 2017; 100:445–453 [View Article] [PubMed]
    [Google Scholar]
  11. Bej AKP DP, Brasher CW, Vickery MC, Jones DD, Kaysner CA. Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh . J Microbiol Methods 1999; 36:215–225
    [Google Scholar]
  12. Lee SE, Ryu PY, Kim SY, Kim YR, Koh JT et al. Production of Vibrio vulnificus hemolysin in vivo and its pathogenic significance. Biochem Biophys Res Commun 2004; 324:86–91 [View Article] [PubMed]
    [Google Scholar]
  13. Esteves K, Mosser T, Aujoulat F, Hervio-Heath D, Monfort P et al. Highly diverse recombining populations of Vibrio cholerae and Vibrio parahaemolyticus in French Mediterranean coastal lagoons. Front Microbiol 2015; 6:708 [View Article] [PubMed]
    [Google Scholar]
  14. Gutierrez West CK, Klein SL, Lovell CR. High frequency of virulence factor genes tdh, trh, and tlh in Vibrio parahaemolyticus strains isolated from a pristine estuary. Appl Environ Microbiol 2013; 79:2247–2252 [View Article] [PubMed]
    [Google Scholar]
  15. Dickerson J, Gooch-Moore J, Jacobs JM, Mott JB. Characteristics of Vibrio vulnificus isolates from clinical and environmental sources. Mol Cell Probes 2021; 56:101695 [View Article] [PubMed]
    [Google Scholar]
  16. Roig FJ, Sanjuan E, Llorens A, Amaro C. pilF polymorphism-based PCR to distinguish Vibrio vulnificus strains potentially dangerous to public health. Appl Environ Microbiol 2010; 76:1328–1333 [View Article] [PubMed]
    [Google Scholar]
  17. Rosche TM, Binder EA, Oliver JD. Vibrio vulnificus genome suggests two distinct ecotypes. Environ Microbiol Rep 2010; 2:128–132 [View Article] [PubMed]
    [Google Scholar]
  18. Faruque S. The biology of Vibrios . Thompson F. eds In The Biology of Vibrios Washington, DC, USA: ASM Press; 2006 pp 385–398
    [Google Scholar]
  19. Thornber K, Verner‐Jeffreys D, Hinchliffe S, Rahman MM, Bass D et al. Evaluating antimicrobial resistance in the global shrimp industry. Rev Aquac 2019; 12:966–986 [View Article] [PubMed]
    [Google Scholar]
  20. FAO FAO yearbook. Fishery and Aquaculture Statistics 2017 / FAO yearbook. Fisheries and aquaculture statistics 2017 / FAO anuario. Rome / Roma: Estadísticas de pesca y acuicultura 2017; 2019
  21. Bostock J, McAndrew B, Richards R, Jauncey K, Telfer T et al. Aquaculture: global status and trends. Philos Trans R Soc Lond B Biol Sci 2010; 365:2897–2912 [View Article] [PubMed]
    [Google Scholar]
  22. MMO UK Sea fisheries statistics 2018 London: Marine Management Organisation; 2019
    [Google Scholar]
  23. Tuševljak NR, Waddell L, Dutil L, Cernicchiaro N, Greig J et al. Prevalence of zoonotic bacteria in wild and farmed aquatic species and seafood: a scoping study, systematic review, and meta-analysis of published research. Foodborne Pathog Dis 2012; 6:487–497
    [Google Scholar]
  24. Yang C, Zhang X, Fan H, Li Y, Hu Q et al. Genetic diversity, virulence factors and farm-to-table spread pattern of Vibrio parahaemolyticus food-associated isolates. Food Microbiol 2019; 84:103270 [View Article] [PubMed]
    [Google Scholar]
  25. Holmstrom K, Graslund S, Wahlstrom A, Poungshompoo S, Bengtsson B-E et al. Antibiotic use in shrimp farming and implications for environmental impacts and human health. Int J Food Sci Technol 2003; 38:255–266 [View Article]
    [Google Scholar]
  26. Henriksson PJG, Rico A, Troell M, Klinger DH, Buschmann AH et al. Unpacking factors influencing antimicrobial use in global aquaculture and their implication for management: a review from a systems perspective. Sustain Sci 2018; 13:1105–1120 [View Article] [PubMed]
    [Google Scholar]
  27. Thi Kim Chi T, Clausen JH, Van PT, Tersbøl B, Dalsgaard A. Use practices of antimicrobials and other compounds by shrimp and fish farmers in Northern Vietnam. Aquaculture Reports 2017; 7:40–47 [View Article]
    [Google Scholar]
  28. Ibrahim M, Ahmad F, Yaqub B, Ramzan A, Imran A et al. Current trends of antimicrobials used in food animals and aquaculture. Antibiotics and Antimicrobial Resistance Genes in the Environment 202039–69
    [Google Scholar]
  29. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A 2018; 115:E70–E3463
    [Google Scholar]
  30. Thongkao K, Sudjaroen Y. Screening of antibiotic resistance genes in pathogenic bacteria isolated from tiny freshwater shrimp (Macrobrachium lanchesteri) and “Kung Ten”, the uncooked Thai food. J Adv Vet Anim Res 2020; 7:83–91 [View Article] [PubMed]
    [Google Scholar]
  31. Jang HM, Kim YB, Choi S, Lee Y, Shin SG et al. Prevalence of antibiotic resistance genes from effluent of coastal aquaculture, South Korea. Environ Pollut 2018; 233:1049–1057 [View Article] [PubMed]
    [Google Scholar]
  32. Janecko N, Martz SL, Avery BP, Daignault D, Desruisseau A et al. Carbapenem-resistant Enterobacter spp. in retail seafood imported from Southeast Asia to Canada. Emerg Infect Dis 2016; 22:1675–1677 [View Article] [PubMed]
    [Google Scholar]
  33. Mok JS, Ryu A, Kwon JY, Park K, Shim KB. Abundance, antimicrobial resistance, and virulence of pathogenic Vibrio strains from molluscan shellfish farms along the Korean coast. Mar Pollut Bull 2019; 149:110559 [View Article] [PubMed]
    [Google Scholar]
  34. Xie T, Wu Q, Xu X, Zhang J, Guo W. Prevalence and population analysis of Vibrio parahaemolyticus in aquatic products from South China markets. FEMS Microbiol Lett 2015; 362:22
    [Google Scholar]
  35. Yang C, Pei X, Wu Y, Yan L, Yan Y et al. Recent mixing of Vibrio parahaemolyticus populations. ISME J 2019; 13:2578–2588 [View Article] [PubMed]
    [Google Scholar]
  36. City Populations United Kingdom, East of England, Norfolk; 2018 https://www.citypopulation.de/php/uk-england-eastofengland.php accessed 17 Apr 2018
  37. Kantar Group and Affiliates Great Britain Grocery Market Share; 2018 www.kantarworldpanel.com/global/grocery-market-share/great-britain/snapshot/22.04.18/ accessed 22 Apr 2018
  38. ISO ISO 21872-1:2017 I. Microbiology of the food chain - Horizontal method for the determination of Vibrio spp. - Part 1: Detection of potentially enteropathogenic Vibrio parahaemolyticus, Vibrio cholerae and Vibrio vulnificus. Switzerland; 2017
  39. Connor TR, Loman NJ, Thompson S, Smith A, Southgate J et al. CLIMB (the Cloud Infrastructure for Microbial Bioinformatics): an online resource for the medical microbiology community. Microb Genom 2016; 2:e000086 [View Article] [PubMed]
    [Google Scholar]
  40. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  41. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  42. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  43. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  44. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  45. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  46. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15: R46 [View Article] [PubMed]
    [Google Scholar]
  47. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: Rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article]
    [Google Scholar]
  48. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
    [Google Scholar]
  49. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
    [Google Scholar]
  50. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: Hierarchical and refined dataset for big data analysis--10 years on. Nucleic Acids Res 2016; 44:D694–7 [View Article]
    [Google Scholar]
  51. Sweeney MT, Lubbers BV, Schwarz S, Watts JL. Applying definitions for multidrug resistance, extensive drug resistance and pandrug resistance to clinically significant livestock and companion animal bacterial pathogens. J Antimicrob Chemother 2018; 73:1460–1463 [View Article] [PubMed]
    [Google Scholar]
  52. Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article] [PubMed]
    [Google Scholar]
  53. Singh DV, Isac SR, Colwell RR. Development of a hexaplex PCR assay for rapid detection of virulence and regulatory genes in Vibrio cholerae and Vibrio mimicus . J Clin Microbiol 2002; 40:4321–4324 [View Article] [PubMed]
    [Google Scholar]
  54. Octavia S, Salim A, Kurniawan J, Lam C, Leung Q et al. Population structure and evolution of non-O1/non-O139 Vibrio cholerae by multilocus sequence typing. PLoS One 2013; 8:e65342 [View Article] [PubMed]
    [Google Scholar]
  55. Gonzalez-Escalona N, Martinez-Urtaza J, Romero J, Espejo RT, Jaykus LA et al. Determination of molecular phylogenetics of Vibrio parahaemolyticus strains by multilocus sequence typing. J Bacteriol 2008; 190:2831–2840 [View Article] [PubMed]
    [Google Scholar]
  56. 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]
  57. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
    [Google Scholar]
  58. Balaban M, Moshiri N, Mai U, Jia X, Mirarab S. TreeCluster: Clustering biological sequences using phylogenetic trees. PLoS One 2019; 14:e0221068 [View Article] [PubMed]
    [Google Scholar]
  59. Tra VT, Meng L, Pichpol D, Pham NH, Baumann M et al. Prevalence and antimicrobial resistance of Vibrio spp. in retail shrimps in Vietnam. Berl Munch Tierarztl Wochenschr 2016; 129:48–51 [PubMed]
    [Google Scholar]
  60. Le Roux F, Blokesch M. Eco-evolutionary dynamics linked to horizontal gene transfer in Vibrios . Annu Rev Microbiol 2018; 72:89–110 [View Article] [PubMed]
    [Google Scholar]
  61. Salomon D, Klimko JA, Trudgian DC, Kinch LN, Grishin NV et al. Type VI secretion system toxins horizontally shared between marine bacteria. PLoS Pathog 2015; 11:e1005128 [View Article] [PubMed]
    [Google Scholar]
  62. Broberg CA, Calder TJ, Orth K. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect 2011; 13:992–1001 [View Article] [PubMed]
    [Google Scholar]
  63. Mejlholm O, Devitt TD, Dalgaard P. Effect of brine marination on survival and growth of spoilage and pathogenic bacteria during processing and subsequent storage of ready-to-eat shrimp (Pandalus borealis . Int J Food Microbiol 2012; 157:16–27 [View Article] [PubMed]
    [Google Scholar]
  64. Letchumanan V, Yin WF, Lee LH, Chan KG. Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shrimps in Malaysia. Front Microbiol 2015; 6:33 [View Article] [PubMed]
    [Google Scholar]
  65. Tan CW, Rukayadi Y, Hasan H, Thung TY, Lee E et al. Prevalence and antibiotic resistance patterns of Vibrio parahaemolyticus isolated from different types of seafood in Selangor, Malaysia. Saudi J Biol Sci 2020; 27:1602–1608 [View Article] [PubMed]
    [Google Scholar]
  66. Vezzulli L, Colwell RR, Pruzzo C. Ocean warming and spread of pathogenic Vibrios in the aquatic environment. Microb Ecol 2013; 65:817–825 [View Article] [PubMed]
    [Google Scholar]
  67. Deeb R, Tufford D, Scott GI, Moore JG, Dow K. Impact of climate change on Vibrio vulnificus abundance and exposure risk. Estuaries Coast 2018; 41:2289–2303 [View Article] [PubMed]
    [Google Scholar]
  68. Hernandez-Cabanyero C, Sanjuan E, Fouz B, Pajuelo D, Vallejos-Vidal E et al. The effect of the environmental temperature on the adaptation to host in the zoonotic pathogen Vibrio vulnificus . Front Microbiol 2020; 11:489 [View Article] [PubMed]
    [Google Scholar]
  69. Froelich BA, Daines DA. In hot water: effects of climate change on Vibrio-human interactions. Environ Microbiol 2020; 22:4101–4111 [View Article] [PubMed]
    [Google Scholar]
  70. Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A et al. Emerging Vibrio risk at high latitudes in response to ocean warming. Nature Climate Change 2012; 3:73–77
    [Google Scholar]
  71. UN World population ageing 2019: highlights. (st/esa/ser.a/430). New York: United Nations Department of Economic and Social Affairs, Population Division; 2019
  72. Campbell-Lendrum D, Woodruff R. Comparative risk assessment of the burden of disease from climate change. Environ Health Perspect 2006; 114:1935–1941 [View Article] [PubMed]
    [Google Scholar]
  73. Jones JL, Ludeke CH, Bowers JC, Garrett N, Fischer M et al. Biochemical, serological, and virulence characterization of clinical and oyster Vibrio parahaemolyticus isolates. J Clin Microbiol 2012; 50:2343–2352 [View Article] [PubMed]
    [Google Scholar]
  74. Garcia K, Torres R, Uribe P, Hernandez C, Rioseco ML et al. Dynamics of clinical and environmental Vibrio parahaemolyticus strains during seafood-related summer diarrhea outbreaks in southern Chile. Appl Environ Microbiol 2009; 75:7482–7487 [View Article] [PubMed]
    [Google Scholar]
  75. Raghunath P. Roles of thermostable direct hemolysin (TDH) and TDH-related hemolysin (TRH) in Vibrio parahaemolyticus . Front Microbiol 2014; 5:805 [View Article] [PubMed]
    [Google Scholar]
  76. Choi Y, Lee Y, Lee S, Kim S, Lee J et al. Microbial contamination including Vibrio cholerae in fishery auction markets in West Sea, South Korea. Fish Aquatic Sci 2019; 22:
    [Google Scholar]
  77. Schwartz K, Hammerl JA, Göllner C, Strauch E. Environmental and clinical strains of Vibrio cholerae non-O1, non-O139 from Germany possess similar virulence gene profiles. Front Microbiol 2019; 10:733 [View Article] [PubMed]
    [Google Scholar]
  78. Mok JS, Ryu A, Kwon JY, Kim B, Park K. Distribution of Vibrio species isolated from bivalves and bivalve culture environments along the Gyeongnam coast in Korea: Virulence and antimicrobial resistance of Vibrio parahaemolyticus isolates. Food Control 2019; 106:
    [Google Scholar]
  79. Semenza JC, Trinanes J, Lohr W, Sudre B, Löfdahl M et al. Environmental suitability of Vibrio infections in a warming climate: An early warning system. Environ Health Perspect 2017; 125:107004 [View Article] [PubMed]
    [Google Scholar]
  80. WHO Critically Important Antimicrobials for Human Medicine, 6th revision . Geneva, Switzerland: World Health Organization; 2019
    [Google Scholar]
  81. Government of Canada Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2017 Guelph: Public Health Agency of Canada; 2019
    [Google Scholar]
  82. CDC National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human isolate surveillance report for 2015. Centers for Disease Control and Prevention; 2018
  83. CDC Cholera and Other Vibrio Illness Surveillance (COVIS): Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Foodborne, Waterborne, and Environmental Diseases; 2019
  84. ECDC Surveillance of antimicrobial resistance in Europe 2018. European Centre for DIsease Prevention and Control. Stockholm; 2019
  85. EMA Sales of veterinary antimicrobial agents in 31 European countries in 2017 (EMA/294674/2019). Amsterdam: European Medicines Agency; 2019
  86. Wong KC, Brown AM, Luscombe GM, Wong SJ, Mendis K. Antibiotic use for Vibrio infections: important insights from surveillance data. BMC Infect Dis 2015; 15:226 [View Article] [PubMed]
    [Google Scholar]
  87. Song EJ, Lee SJ, Lim HS, Kim JS, Jang KK et al. Vibrio vulnificus VvhA induces autophagy-related cell death through the lipid raft-dependent c-Src/NOX signaling pathway. Sci Rep 2016; 6:27080 [View Article] [PubMed]
    [Google Scholar]
  88. Wright AC, Morris JG Jr. The extracellular cytolysin of Vibrio vulnificus: inactivation and relationship to virulence in mice. Infect Immun 1991; 59:192–197 [View Article] [PubMed]
    [Google Scholar]
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