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Environmental Science and Pollution Research

, Volume 26, Issue 20, pp 21034–21043 | Cite as

Occurrence, virulence, and antimicrobial resistance of Vibrio parahaemolyticus isolated from bivalve shellfish farms along the southern coast of Korea

  • A. Ra Ryu
  • Jong Soo MokEmail author
  • Da Eun Lee
  • Ji Young Kwon
  • Kunbawui Park
Short Research and Discussion Article
  • 99 Downloads

Abstract

Vibrio parahaemolyticus is the most common pathogen causing seafood-borne illnesses in Korea. The present study evaluated the occurrence, virulence, and antimicrobial resistance of V. parahaemolyticus in seawater and bivalves obtained in 2016 from the southern coast of Korea, an important region for commercial aquaculture industries, especially the Korean raw seafood culture. V. parahaemolyticus was detected in 87 of 160 (54.4%) bivalve samples and in 32 of 130 (24.5%) seawater samples. Especially high levels were detected during summer to early autumn. All the seawater and bivalves contained less than 2 and 5% of the tdh and trh genes of the isolates, respectively, and seawater isolates possessed two fewer genes than the bivalve isolates. Of 23 antimicrobials tested, three agents (ofloxacin, norfloxacin, and trimethoprim/sulfamethoxazole) effectively treated V. parahaemolyticus illness due to the sensitivity of the isolates. The isolates were highly resistant to ampicillin, however, excluding it as a treatment option. More than half of the isolates exhibited resistance to at least three antimicrobials. These findings indicate the importance of an integrated monitoring and surveillance program noting the occurrence, virulence, and antimicrobial resistance patterns of V. parahaemolyticus in various aquatic sources for preventing human health risks from seafood consumption.

Keywords

Vibrio parahaemolyticus Virulence Antimicrobial resistance Korea Bivalve shellfish Seawater 

Notes

Funding information

This work was supported by a grant from the National Institute of Fisheries Science in Korea (R2018061).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11356_2019_5426_MOESM1_ESM.docx (80 kb)
ESM 1 (DOCX 79 kb)

References

  1. Aarestrup FM, Wegener HC (1999) The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli. Microbes Infect 1:639–644CrossRefGoogle Scholar
  2. Al-Othrubi SM, Kqueen CY, Mirhosseini H, Hadi YA, Radu S (2014) Antibiotic resistance of Vibrio parahaemolyticus isolated from cockles and shrimp sea food marketed in Selangor, Malaysia. Clin Microbiol 3:148–154Google Scholar
  3. Banerjee SK, Farber JM (2018) Trend and pattern of antimicrobial resistance in molluscan Vibrio species sourced to Canadian estuaries. Antimicrob Agents Chemother 62:e00799–e00718CrossRefGoogle Scholar
  4. Burkhardt W, Calci KR (2000) Selective accumulation may account for shellfish-associated viral illness. Appl Environ Microbiol 66:1375–1378CrossRefGoogle Scholar
  5. Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144CrossRefGoogle Scholar
  6. CLSI (Clinical and Laboratory Standard Institute) (2016) Performance standards for antimicrobial susceptibility testing, 26th edn. CLSI supplement M100S. Clinical and Laboratory Standard Institute, Wayne, PA, USAGoogle Scholar
  7. Elmahdi S, DaSilva LV, Parveen S (2016) Antibiotic resistance of Vibrio parahaemolyticus and Vibrio vulnificus in various countries: a review. Food Microbiol 57:128–134CrossRefGoogle Scholar
  8. Ferrini AM, Mannoni V, Suffredini E, Cozzi L, Croci L (2008) Evaluation of antibacterial resistance in Vibrio strains isolated from imported seafood and Italian aquaculture settings. Food Anal Methods 1:164–170CrossRefGoogle Scholar
  9. Gutierrez West CK, Klein SL, Lovell CR (2013) High frequency of virulence factor genes tdh, trh, and tlh in Vibrio parahaemolyticus strains isolated from a pristine estuary. Appl Environ Microbiol 79:2247–2252CrossRefGoogle Scholar
  10. Han F, Walker RD, Janes ME, Prinyawiwatkul W, Ge B (2007) Antimicrobial susceptibilities of Vibrio parahaemolyticus and Vibrio vulnificus isolated from Louisiana Gulf and retail raw oysters. Appl Environ Microbiol 73:7096–7098CrossRefGoogle Scholar
  11. Joseph SW, Colwell RR, Kaper JB (1982) Vibrio parahaemolyticus and related halophilic vibrios. Crit Rev Microbiol 10:77–124CrossRefGoogle Scholar
  12. Kang CH, Shin YJ, Kim WR, Kim YG, Song KC, Oh EG, Kim SK, Yu HS, So JS (2016) Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from oysters in Korea. Environ Sci Pollut Res 23:918–926CrossRefGoogle Scholar
  13. Kang CH, Shin YJ, Jang SC, Yu HS, Kim SK, An SR, Park K, So JS (2017) Characterization of Vibrio parahaemolyticus isolated from oysters in Korea: resistance to various antibiotics and prevalence of virulence genes. Mar Pollut Bull 118:261–266CrossRefGoogle Scholar
  14. Kim SK, An SR, Park BM, Oh EG, Song KC, Kim JW, Yu HS (2016a) Virulence factors and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from oyster Crassostrea gigas. Kor J Fish Aquat Sci 49:116–123Google Scholar
  15. Kim TO, Eum IS, Kim HD, Park KS (2016b) Antimicrobial resistance and minimum inhibitory concentrations of Vibrio parahaemolyticus strains isolated from Gomso Bay, Korea. Kor J Fish Aquat Sci 49:582–588Google Scholar
  16. Kim JH, Shim KB, Shin SB, Park K, Oh EG, Son KT, Yu HS, Lee HJ, Mok JS (2017) Comparison of bioaccumulation and elimination of Escherichia coli and male-specific bacteriophages by ascidians and bivalves. Environ Sci Pollut Res 24:28268–28276CrossRefGoogle Scholar
  17. KMFDS (Korea Ministry of Food and Drug Safety) (2018) Food poisoning outbreak statistics. http://www.mfds.go.kr/fm/index.do. Accessed 14 Aug 2018
  18. Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46:165–170Google Scholar
  19. Lesmana M, Subekti D, Simanjuntak CH, Tjaniadi P, Campbell JR, Oyofo BA (2001) Vibrio parahaemolyticus associated with cholera-like diarrhea among patients in North Jakarta, Indonesia. Diagn Microbiol Infect Dis 39:71–75CrossRefGoogle Scholar
  20. Letchumanan V, Chan KG, Lee LH (2014) Vibrio parahaemolyticus: a review on the pathogenesis, prevalence, and advance molecular identification techniques. Front Microbiol 5:705CrossRefGoogle Scholar
  21. Mazel D, Davies J (1999) Antibiotic resistance in microbes. Cell Mol Life Sci 56:742–754CrossRefGoogle Scholar
  22. MOF (Ministry of Oceans and Fisheries) (2015) Korean shellfish sanitation program (KSSP) FY 2014 annual report. Ministry of Oceans and Fisheries, SejongGoogle Scholar
  23. Mok JS, Lee KJ, Kim PH, Lee TS, Lee HJ, Jung YJ, Kim JH (2016) Bacteriological quality evaluation of seawater and oysters from the Jaranman-Saryangdo area, a designated shellfish growing area in Korea: impact of inland pollution sources. Mar Pollut Bull 108:147–154CrossRefGoogle Scholar
  24. Morris JG, Tenny J (1985) Antibiotic therapy for Vibrio vulnificus infection. J Am Med Assoc 253:1121–1122CrossRefGoogle Scholar
  25. Nishibuchi M, Ishibashi M, Takeda Y, Kaper JB (1985) Detection of the thermostable direct hemolysin gene and related DNA sequences in Vibrio parahaemolyticus and other Vibrio species by the DNA colony hybridization test. Am Soc Microbiol 49:481–486Google Scholar
  26. Oh EG, Son KT, Yu HS, Lee TS, Lee HJ, Shin SB, Kwon JY, Park K, Kim JH (2011) Antimicrobial resistance of Vibrio parahaemolyticus and Vibrio alginolyticus strains isolated from farmed fish in Korea during 2005–2007. J Food Prot 74:380–386CrossRefGoogle Scholar
  27. Ottaviani D, Susini F, Montagna C, Monno R, D'Annibale L (2013) Extensive investigation of antimicrobial resistance in Vibrio parahaemolyticus from shellfish and clinical sources, Italy. Int J Antimicrob Agents 42:191–193CrossRefGoogle Scholar
  28. Park YS, Park K, Kwon JY, Yu HS, Lee HJ, Kim JH, Lee TS, Kim PH (2016) Antimicrobial resistance and distribution of virulence factors of Vibrio parahaemolyticus isolated from shellfish farms on the southern coast of Korea. Kor J Fish Aquat Sci 49:460–466Google Scholar
  29. Park K, Mok JS, Kwon JY, Ryu AR, Kim SH, Lee HJ (2018a) Food-borne outbreaks, distributions, virulence, and antibiotic resistance profiles of Vibrio parahaemolyticus in Korea from 2003 to 2016: a review. Fish Aquat Sci 21:3CrossRefGoogle Scholar
  30. Park K, Mok JS, Ryu AR, Kwon JY, Ham IT, Shim KB (2018b) Occurrence and virulence of Vibrio parahaemolyticus isolated from seawater and bivalve shellfish of the Gyeongnam coast, Korea, in 2004–2016. Mar Pollut Bull 137:382–387CrossRefGoogle Scholar
  31. Shaw KS, Goldstein RER, He X, Jacobs JM, Crump BC, Sapkota AR (2014) Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland Coastal Bays. PLoS One 9:1–11Google Scholar
  32. Shimohata T, Takahashi A (2010) Diarrhea induced by infection of Vibrio parahaemolyticus. J Med Investig 57:179–182CrossRefGoogle Scholar
  33. Silva IP, Carneiro CS, Saraiva MAF, Oliveira TAS, Sousa OV, Evangelista-Barreto NS (2018) Antimicrobial resistance and potential virulence of Vibrio parahaemolyticus isolated from water and bivalve mollusks from Bahia, Brazil. Mar Pollut Bull 131:757–762CrossRefGoogle Scholar
  34. Son KT, Oh EG, Lee TS, Lee HJ, Kim PH, Kim JH (2005) Antimicrobial susceptibility of Vibrio parahaemolyticus and Vibrio alginolyticus from fish farms on the southern coast of Korea. J Kor Fish Soc 38:365–371Google Scholar
  35. Su YC, Liu C (2007) Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol 24:549–558CrossRefGoogle Scholar
  36. Thompson FL, Iida T, Swings J (2004) Biodiversity of vibrios. Microbiol Mol Biol Rev 68:403–431CrossRefGoogle Scholar
  37. Titilawo Y, Sibanda T, Obi L, Okoh A (2015) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of water. Environ Sci Pollut Res 22:10969–10980CrossRefGoogle Scholar
  38. U.S. Food and Drug Administration (US FDA) (2018) Bacteriological analytical manual. https://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm2006949.htm. Accessed 19 Oct 2018
  39. WHO (World Health Organization) (2014) Antimicrobial resistance: global report on surveillance 2014. http://www.who.int/drugresistance/documents/surveillancereport/en/. Accessed 28 March 2017
  40. Xie T, Wu Q, Zhang J, Xu X, Cheng J (2017) Comparison of Vibrio parahaemolyticus isolates from aquatic products and clinical by antibiotic susceptibility, virulence, and molecular characterization. Food Control 71:315–321CrossRefGoogle Scholar
  41. Yang JH, Mok JS, Jung YJ, Lee KJ, Kwon JY, Park K, Moon SY, Kwon SJ, Ryu AR, Lee TS (2017) Distribution and antimicrobial susceptibility of Vibrio species associated with zooplankton in coastal area of Korea. Mar Pollut Bull 125:39–44CrossRefGoogle Scholar
  42. Yu HS, Oh EG, Shin SB, Park YS, Lee HJ, Kim JH, Song KC (2014) Distribution and antimicrobial resistance of Vibrio parahaemolyticus isolated from Korean shellfish. Kor J Fish Aquat Sci 47:508–515Google Scholar
  43. Yu Q, Niu M, Yu M, Liu Y, Wang D, Shi X (2016) Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shellfish in Shanghai. Food Control 60:263–268CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Food Safety and Processing Research DivisionNational Institute of Fisheries ScienceBusanRepublic of Korea
  2. 2.Southeast Sea Fisheries Research InstituteNational Institute of Fisheries SciencesTongyeongRepublic of Korea

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