Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Isolation, Molecular Characterization and Antibiotic Susceptibility Pattern of Vibrio parahaemolyticus from Aquatic Products in the Southern Fujian Coast, China

  • Hu, Yuanqing (School of Biological Science and Biotechnology, Minnan Normal University) ;
  • Li, Fengxia (School of Biological Science and Biotechnology, Minnan Normal University) ;
  • Zheng, Yixian (School of Biological Science and Biotechnology, Minnan Normal University) ;
  • Jiao, Xinan (Jiangsu Key Laboratory of Zoonosis, Yangzhou University) ;
  • Guo, Liqing (Zhangzhou Center for Disease Control and Prevention)
  • Received : 2020.01.03
  • Accepted : 2020.02.24
  • Published : 2020.06.28
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Abstract

Vibrio parahaemolyticus is a major gastroenteritis-causing pathogen in many Asian countries. Antimicrobial resistance in V. parahaemolyticus has been recognized as a critical threat to food safety. In this study, we determined the prevalence and incidence of antimicrobial resistance in V. parahaemolyticus in the southern Fujian coast, China. A total of 62 isolates were confirmed in retail aquatic products from June to October of 2018. The serotype O3:K6 strains, the virulence genes tdh and trh, antibiotic susceptibility and molecular typing were investigated. Then plasmid profiling analysis and curing experiment were performed for multidrug-resistant strains. The results showed that the total occurrence of V. parahaemolyticus was 31% out of 200 samples. Five strains (8.1%) out of 62 isolates were identified as the V. parahaemolyticus O3:K6 pandemic clone. A large majority of isolates exhibited higher resistance to penicillin (77.4%), oxacillin (71%), ampicillin (66.1%) and vancomycin (59.7%). Seventy-one percent (44/62) of the isolates exhibited multiple antimicrobial resistance. All 62 isolates were grouped into 7 clusters by randomly amplified polymorphic DNA, and most of the isolates (80.6%) were distributed within cluster A. Plasmids were detected in approximately 75% of the isolates, and seven different profiles were observed. Seventy-six percent (25/33) of the isolates carrying the plasmids were eliminated by 0.006% SDS incubated at 42℃, a sublethal condition. The occurrence of multidrug-resistant strains could be an indication of the excessive use of antibiotics in aquaculture farming. The rational use of antimicrobial agents and the surveillance of antibiotic administration may reduce the acquisition of resistance by microorganisms in aquatic ecosystems.

Keywords

References

  1. Elmahdi S, Dasilva LV, Parveen S. 2016. Antibiotic resistance of Vibrio parahaemolyticus and Vibrio vulnificus in various countries: a review. Food Microbiol. 57: 128-134. https://doi.org/10.1016/j.fm.2016.02.008
  2. Lou Y, Liu HQ, Zhang ZH, Pan YJ, Zhao Y. 2016. Mismatch between antimicrobial resistance phenotype and genotype of pathogenic Vibrio parahaemolyticus isolated from seafood. Food Control 59: 207-211. https://doi.org/10.1016/j.foodcont.2015.04.039
  3. Kang CH, Shin YJ, Kim WR, Kim YG, Song KC, Oh EG, et al. 2016. Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from oysters in Korea. Environ. Sci. Pollut. R. 23: 918-926. https://doi.org/10.1007/s11356-015-5650-9
  4. Xie TF, Xu XK, Wu QP, Zhang JM, Cheng JH. 2016. Prevalence, molecular characterization, and antibiotic susceptibility of Vibrio parahaemolyticus from ready-to-eat foods in China. Front. Microbiol. 7: 549.
  5. Odeyemi OA, Stratev D. 2016. Occurrence of antimicrobial resistant or pathogenic Vibrio parahaemolyticus in seafood. A mini review. Rev. Med. Vet. 67: 93-98.
  6. He Y, Jin LL, Sun FJ, Hu QX, Chen LM. 2016. Antibiotic and heavy-metal resistance of Vibrio parahaemolyticus isolated from fresh shrimps in Shanghai fish markets, China. Environ. Sci. Pollut. Res. Int. 23: 15033-15040. https://doi.org/10.1007/s11356-016-6614-4
  7. Li H, Tang R, Lou Y, Cui ZL, Chen WJ, Hong Q, et al. 2017. A comprehensive epidemiological research for clinical Vibrio parahaemolyticus in Shanghai. Front. Microbiol. 8: 1043. https://doi.org/10.3389/fmicb.2017.01043
  8. Yu QQ, Niu MY, Yu MQ, Liu YH, Wang DP, Shi XM. 2016. Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shellfish in Shanghai. Food Control 60: 263-268. https://doi.org/10.1016/j.foodcont.2015.08.005
  9. Ahmed HA, El RB, Hussein MA, Khedr M, Abo ER, Elashram A. 2018. Molecular characterization, antibiotic resistance pattern and biofilm formation of Vibrio parahaemolyticus and V. cholerae isolated from crustaceans and humans. Int. J. Food Microbiol. 274: 31-37. https://doi.org/10.1016/j.ijfoodmicro.2018.03.013
  10. Han DS, Tang H, Ren CL, Wang GZ, Zhou L, Han CX. 2015. Prevalence and genetic diversity of clinical Vibrio parahaemolyticus isolates from China, revealed by multilocus sequence typing scheme. Front. Microbiol. 6: 291. https://doi.org/10.3389/fmicb.2015.00291
  11. Lopatek M, Wieczorek K, Osek J. 2018. Antimicrobial resistance, virulence factors, and genetic profiles of Vibrio parahaemolyticus from seafood. Appl. Environ. Microbiol. 84: e00537-00518.
  12. Paydar M, Teh CSJ, Thong KL. 2013. Prevalence and characterisation of potentially virulent Vibrio parahaemolyticus in seafood in Malaysia using conventional methods, PCR and REP-PCR. Food Control 32: 13-18. https://doi.org/10.1016/j.foodcont.2012.11.034
  13. Xie TF, Wu QP, Xu XK, Zhang JM, Guo WP. 2015. Prevalence and population analysis of Vibrio parahaemolyticus in aquatic products from South China markets. FEMS Microbiol. Lett. 362: fnv178. https://doi.org/10.1093/femsle/fnv178
  14. Chao GX, Jiao XN, Zhou XH, Yang ZQ, Huang JL, Zhou LP, et al. 2009. Distribution, prevalence, molecular typing, and virulence of Vibrio parahaemolyticus isolated from different sources in coastal province Jiangsu, China. Food Control 20: 907-912. https://doi.org/10.1016/j.foodcont.2009.01.004
  15. Maluping RP, Ravelo C, Lavilla-Pitogo CR, Krovacek K, Romalde JL. 2005. Molecular typing of Vibrio parahaemolyticus strains isolated from the Philippines by PCR-based methods. J. Appl. Microbiol. 99: 383-391. https://doi.org/10.1111/j.1365-2672.2005.02571.x
  16. Zhao F, Zhou DQ, Cao HH, Ma LP, Jiang YH. 2011. Distribution, serological and molecular characterization of Vibrio parahaemolyticus from shellfish in the eastern coast of China. Food Control 22: 1095-1100. https://doi.org/10.1016/j.foodcont.2010.12.017
  17. Marhual NP, Das BK, Samal SK. 2012. Characterization of Vibrio alginolyticus and Vibrio parahaemolyticus isolated from Penaeus monodon: antimicrobial resistance, plasmid profiles and random amplification of polymorphic DNA analysis. Afr. J. Microbiol. Res. 6: 4261-4269.
  18. Li RC, Chiou JC, Chan EW, Chen S. 2016. A novel PCR-based approach for accurate identification of Vibrio parahaemolyticus. Front. Microbiol. 7: 44. https://doi.org/10.3389/fmicb.2016.00044
  19. Alaboudi AR, Ababneh M, Osaili TM, Shloul KA. 2016. Detection, identification, and prevalence of pathogenic Vibrio parahaemolyticus in fish and coastal environment in Jordan. J. Food Sci. 81: M130-M134. https://doi.org/10.1111/1750-3841.13151
  20. 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: 757-762. https://doi.org/10.1016/j.marpolbul.2018.05.007
  21. Xu XK, Wu QP, Zhang JM, Cheng JH, Zhang SH, Wu K. 2014. Prevalence, pathogenicity, and serotypes of Vibrio parahaemolyticus in shrimp from Chinese retail markets. Food Control 46: 81-85. https://doi.org/10.1016/j.foodcont.2014.04.042
  22. Caburlotto G, Gennari M, Ghidini V, Tafi M, Lleo MM. 2010. Serological and molecular characterization of Vibrio parahaemolyticus marine strains carrying pandemic genetic markers. ISME J. 4: 1071-1074. https://doi.org/10.1038/ismej.2010.34
  23. Masatoshi O, Ro O, Akihiko T, Masatomo M, Eiji A, Haruo W. 2010. Genetic analyses of the putative O and K antigen gene clusters of pandemic Vibrio parahaemolyticus. Microbiol. Immunol. 52: 251-264. https://doi.org/10.1111/j.1348-0421.2008.00027.x
  24. Zhang YY, Mei LL, Zhang JY, Zhan L, Chen JC, Chen HH, et al. 2016. Triplex PCR method for Vibrio parahemolyticus serotype O3:K6 strains detection. Chinese J. Zoonoses 32: 632-635.
  25. Yukiko HK, Kanji S, Mitsuaki N, Ashrafuzzaman C, Jun Y, Yoshimitsu O, et al. 2003. Prevalence of pandemic thermostable direct hemolysin-producing Vibrio parahaemolyticus O3:K6 in seafood and the coastal environment in Japan. Appl. Environ. Microbiol. 69: 3883-3891. https://doi.org/10.1128/AEM.69.7.3883-3891.2003
  26. Ghenem L, Elhadi N. 2018. Isolation, molecular characterization, and antibiotic resistance patterns of Vibrio parahaemolyticus isolated from coastal water in the Eastern Province of Saudi Arabia. J. Water Health 16: 57-69. https://doi.org/10.2166/wh.2017.361
  27. Lou K, Ban R, Zhao XM. 2002. Curing of the Bacillus subtilis plasmid using sodium dodecyl sulfate. transactions of Tianjin University. 8: 148-151.
  28. Devi R, Surendran PK, Chakraborty K. 2009. Antibiotic resistance and plasmid profiling of Vibrio parahaemolyticus isolated from shrimp farms along the southwest coast of India. World J. Microbiol. Biotechnol. 25: 2005-2012. https://doi.org/10.1007/s11274-009-0101-8
  29. Jiang YH, Chu YB, Xie GS, Li FL, Wang LZ, Huang J, et al. 2019. Antimicrobial resistance, virulence and genetic relationship of Vibrio parahaemolyticus in seafood from coasts of Bohai Sea and Yellow Sea, China. Int. J. Food Microbiol. 290: 116-124. https://doi.org/10.1016/j.ijfoodmicro.2018.10.005
  30. Pan H, Paudyal N, Li XL, Fang WH, Yue M. 2018. Multiple food-animal-borne route in transmission of antibiotic-resistant Salmonella Newport to humans. Front. Microbiol. 9: 23. https://doi.org/10.3389/fmicb.2018.00023
  31. Chen J, Zhang RH, Qi XJ, Zhou B, Wang JK, Chen Y, et al. 2017. Epidemiology of foodborne disease outbreaks caused by Vibrio parahaemolyticus during 2010-2014 in Zhejiang Province, China. Food Control 77: 110-115. https://doi.org/10.1016/j.foodcont.2017.02.004
  32. Sperling L, Alter T, Huehn S. 2015. Prevalence and antimicrobial resistance of Vibrio spp. in retail and farm shrimps in Ecuador. J. Food Prot. 78: 2089-2092. https://doi.org/10.4315/0362-028X.JFP-15-160
  33. Chen SY, Ge BL. 2010. Development of a toxR-based loop-mediated isothermal amplification assay for detecting Vibrio parahaemolyticus. BMC Microbiol. 10: 41. https://doi.org/10.1186/1471-2180-10-41
  34. Chiou JC, Li RC, Chen S. 2015. CARB-17 family of $\beta$-lactamases mediates intrinsic resistance to penicillins in Vibrio parahaemolyticus. Antimicrob. Agents Chmother. 59: 3593-3595. https://doi.org/10.1128/AAC.00047-15
  35. Han DS, Yu F, Tang H, Ren CL, Wu CY, Zhang P, et al. 2017. Spreading of pandemic Vibrio parahaemolyticus O3:K6 and its serovariants: a re-analysis of strains isolated from multiple studies. Front. Cell. Infect. Mi. 7: 188. https://doi.org/10.3389/fcimb.2017.00188
  36. Hernandezdiaz LDJ, Leonsicairos N, Velazquezroman J, Floresvillasenor H, Guadronllanos AM, Martinezgarcia JJ, et al. 2015. A pandemic Vibrio parahaemolyticus O3:K6 clone causing most associated diarrhea cases in the Pacific Northwest coast of Mexico. Front. Microbiol. 6: 221. https://doi.org/10.3389/fmicb.2015.00221
  37. Ma C, Deng XL, Ke CW, He DM, Liang ZM, Li W, et al. 2014. Epidemiology and etiology characteristics of foodborne outbreaks caused by Vibrio parahaemolyticus during 2008-2010 in Guangdong Province, China. Foodborne Pathog. Dis. 11: 21-29. https://doi.org/10.1089/fpd.2013.1522
  38. Zhang HZ, Sun SF, Shi WM, Cui L, Gu QF. 2013. Serotype, virulence, and genetic traits of foodborne and clinical Vibrio parahaemolyticus isolates in Shanghai, China. Foodborne Pathog. Dis. 10: 796-804. https://doi.org/10.1089/fpd.2012.1378
  39. Yang ZQ, Jiao XA, Zhou XH, Cao GX, Fang WM, Gu RX. 2008. Isolation and molecular characterization of Vibrio parahaemolyticus from fresh, low-temperature preserved, dried, and salted seafood products in two coastal areas of eastern China. Int. J. Food Microbiol. 125: 279-285. https://doi.org/10.1016/j.ijfoodmicro.2008.04.007
  40. Parvathi A, Kumar HS, Bhanumathi A, Ishibashi M, Nishibuchi M, Karunasagar I, et al. 2010. Molecular characterization of thermostable direct haemolysin-related haemolysin (TRH)-positive Vibrio parahaemolyticus from oysters in Mangalore, India. Environ. Microbiol. 8: 997-1004. https://doi.org/10.1111/j.1462-2920.2006.00990.x
  41. Sahilah AM, Laila RAS, Sallehuddin HM, Osman H, Aminah A, Azuhairi AA. 2014. Antibiotic resistance and molecular typing among cockle (Anadara granosa) strains of Vibrio parahaemolyticus by polymerase chain reaction (PCR)-based analysis. World J. Microbiol. Biotechnol. 30: 649-659. https://doi.org/10.1007/s11274-013-1494-y
  42. Tunung R, Jeyaletchumi P, Noorlis A, Tang YH, Sandra A, Ghazali FM, et al. 2012. Biosafety of Vibrio parahaemolyticus from vegetables based on antimicrobial sensitivity and RAPD profiling. Int. Food Res. J. 19: 467-474.
  43. Vazquez-Sanchez D, Lopez-Cabo M, Saa-Ibusquiza P, Rodriguez-Herrera JJ. 2012. Incidence and characterization of Staphylococcus aureus in fishery products marketed in Galicia (Northwest Spain). Int. J. Food Microbiol. 157: 286-296. https://doi.org/10.1016/j.ijfoodmicro.2012.05.021
  44. Noorlis A, Ghazali FM, Cheah YK, Zainazor TCT, Ponniah J, Tunung R, et al. 2011. Prevalence and quantification of Vibrio species and Vibrio parahaemolyticus in freshwater fish at hypermarket level. Int. Food Res. J. 18: 689-695.
  45. Zarei M, Borujeni MP, Jamnejad A, Khezrzadeh M. 2012. Seasonal prevalence of Vibrio species in retail shrimps with an emphasis on Vibrio parahaemolyticus. Food Control 25: 107-109. https://doi.org/10.1016/j.foodcont.2011.10.024
  46. Kang CH, Shin YJ, Jang SC, Yu HS, Kim SK, An S, et al. 2017. Characterization of Vibrio parahaemolyticus isolated from oysters in Korea: Resistance to various antibiotics and prevalence of virulence genes. Mar. Pollut. Bull. 118: 261-266. https://doi.org/10.1016/j.marpolbul.2017.02.070
  47. Letchumanan V, Yin WF, Lee LH, Chan KG. 2015. Prevalence and antimicrobial susceptibility of Vibrio parahaemolyticus isolated from retail shrimps in Malaysia. Front. Microbiol. 6: 33. https://doi.org/10.3389/fmicb.2015.00033
  48. Al-Hasnawy HH, Jodi MR, Hamza HJ. 2018. Molecular characterization and sequence analysis of plasmid-mediated quinolone resistance genes in extended-spectrum beta-lactamases producing uropathogenic Escherichia coli in Babylon Province, Iraq. Rev. Med. Microbiol. 29: 129-135. https://doi.org/10.1097/MRM.0000000000000136
  49. Jiang Y, Yao L, Li F, Tan Z, Zhai Y, Wang L. 2014. Characterization of antimicrobial resistance of Vibrio parahaemolyticus from cultured sea cucumbers (A postichopus japonicas). Lett. Appl. Microbiol. 59: 147-154. https://doi.org/10.1111/lam.12258
  50. Xu XK, Cheng JH, Wu QP, Zhang JM, Xie TF. 2016. Prevalence, characterization, and antibiotic susceptibility of Vibrio parahaemolyticus isolated from retail aquatic products in North China. BMC Microbiol. 16: 32. https://doi.org/10.1186/s12866-016-0650-6
  51. Zhao S, Ma LC, Wang Y, Fu GH, Zhou JF, Li XC, et al. 2018. Antimicrobial resistance and pulsed-field gel electrophoresis typing of Vibrio parahaemolyticus isolated from shrimp mariculture environment along the east coast of China. Mar. Pollut. Bull. 136: 164-170. https://doi.org/10.1016/j.marpolbul.2018.09.017
  52. Tunung R, Margaret S, Jeyaletchumi P, Chai LC, Tuan Zainazor TC, Ghazali FM, et al. 2010. Prevalence and quantification of Vibrio parahaemolyticus in raw salad vegetables at retail level. J. Microbiol. Biotechnol. 20: 391-396. https://doi.org/10.4014/jmb.0908.08009
  53. Daramola BA, Williams R, Dixon RA. 2009. In vitro antibiotic susceptibility of Vibrio parahaemolyticus from environmental sources in northern England. Int. J. Antimicrob. Agents 34: 499-500. https://doi.org/10.1016/j.ijantimicag.2009.06.015
  54. 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: e89616. https://doi.org/10.1371/journal.pone.0089616
  55. Yano Y, Hamano K, Satomi M, Tsutsui I, Ban M, Aue-Umneoy D. 2014. Prevalence and antimicrobial susceptibility of Vibrio species related to food safety isolated from shrimp cultured at inland ponds in Thailand. Food Control 38: 30-36. https://doi.org/10.1016/j.foodcont.2013.09.019
  56. Silvester R, Alexander D. 2015. Prevalence, antibiotic resistance, virulence and plasmid profiles of Vibrio parahaemolyticus from a tropical estuary and adjoining traditional prawn farm along the southwest coast of India. Ann. Microbiol. 65: 2141-2149. https://doi.org/10.1007/s13213-015-1053-x
  57. Zhang RF, Wang YL, Gu JD. 2006. Identification of environmental plasmid-bearing Vibrio species isolated from polluted and pristine marine reserves of Hong Kong, and resistance to antibiotics and mercury. Antonie Van Leeuwenhoek 89: 307-315. https://doi.org/10.1007/s10482-005-9032-z

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