Article history: Received: 04-06-2017, Accepted: 27-07-2018, Published online: 18-09-2018
Corresponding author: Binaya Bhusan Nayak
E-mail: firstname.lastname@example.orgCitation: Lekshmi M, Das O, Kumar S, Nayak BB (2018) Occurrence of human enterovirus in tropical fish and shellfish and their relationship with fecal indicator bacteria, Veterinary World, 11(9): 1285-1290.
Aim: Human enteroviruses in fish and shellfish are a health concern worldwide. Human infections occur due to the consumption of raw or insufficiently cooked fish or shellfish. The objective of this study was to determine the occurrence of human enteric viruses belonging to Enterovirus (EV) group in seafood in Mumbai and to correlate their occurrence with the bacterial indicators of fecal contamination.
Materials and Methods: Samples of fresh fish and shellfish collected from fish landing centers and retail fish markets were analyzed by virus concentration, nucleic acid extraction, and reverse transcription-polymerase chain reaction (RT-PCR). Bacterial indicators of fecal contamination were estimated by the most probable number technique. The relationship between the presence of virus and fecal indicators was determined by statistical analysis.
Results: A total of 89 samples comprising of fish, shrimps, oysters, clams, and mussels were screened in this study. EV was detected in 32 (35.95%) samples, and all the virus-positive samples belonged to bivalve molluscan group. None of the finfish and crustacean shellfish samples was positive for the enteric viruses. Clams were found to be the most contaminated with 48.4% of the samples being positive for EV. The prevalence of enteric viruses in seafood samples showed a strong positive correlation with the bacteriological indicators of fecal contamination, suggesting that fecal coliform bacteria are good indicators of EVs in tropical seafood.
Conclusion: The presence of EVs in seafood is a public health hazard. Increasing level of coastal water contamination from anthropogenic sources is the primary reason for the contamination of seafood with EVs. Continuous monitoring of coastal waters and seafood for enteric viruses will help to ensure the safety of fish and shellfish for human consumption.
Keywords: coliforms, enterovirus, fish, indicator bacteria, reverse transcription-polymerase chain reaction, shellfish.
1. Richards, G.P. (2016) Shellfish-associated enteric virus illness: Virus localization, disease outbreaks and prevention. In: Goyal, S., Cannon, J., editors. Viruses in Foods. Food Microbiology and Food Safety. Springer, Cham.
2. Connell, C., Tong, H.I., Wang, Z., Allmann, E. and Lu, Y. (2012) New approaches for enhanced detection of enteroviruses from Hawaiian environmental waters. PLoS One, 7: 1-9. [Crossref] [PubMed] [PMC]
4. Hellmer, M., Paxeus, N., Magnius, L., Enache, L., Arnholm, B., Johansson, A., Bergstrom, T. and Norder, H. (2014) Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Appl. Environ. Microbiol., 80: 6771-6781. [Crossref] [PubMed] [PMC]
5. Greening, G.E. and Cannon, J.L. (2016) Human and animal viruses in food (including taxonomy of enteric viruses). In: Goyal, S., Cannon, J., editors. Viruses in Foods. Food Microbiology and Food Safety. Springer, Cham.
6. Huang, W., Wang, G., Zhuge, J., Nolan, S.M., Dimitrova, N. and Fallon, J.T. (2015) Whole-genome sequence analysis reveals the enterovirus D68 isolates during the United States 2014 outbreak mainly belong to a novel clade. Sci. Rep., 5: 15223. [Crossref] [PubMed] [PMC]
7. Piralla, A., Daleno, C., Scala, A., Greenberg, D., Usonis, V., Principi, N., Baldanti, F. and Esposito, S. (2013) Genome characterisation of enteroviruses 117 and 118: A new group within human enterovirus species C. PLoS One, 8: e60641. [Crossref] [PubMed] [PMC]
8. Hassard, F., Gwyther, C.L., Farkas, K., Andrews, A., Jones, V., Cox, B., Brett, H., Jones, D.L., McDonald, J.E. and Malham, S.K. (2016) Abundance and distribution of enteric bacteria and viruses in coastal and estuarine sediments-a review. Front Microbiol., 7: 1692. [Crossref] [PubMed] [PMC]
9. Umesha, K.R., Bhavani, N.C., Venugopal, M.N., Karunasagar, I., Krohne, G. and Karunasagar, I. (2008) Prevalence of human pathogenic enteric viruses in bivalve molluscan shellfish and cultured shrimp in South West coast of India. Int. J. Food Microbiol., 122: 279-286. [Crossref] [PubMed]
10. Suffredini, E., Corrain, C., Arcangeli, G., Fasolato, L., Manfrin, A., Rossetti, E., Biazzi, E., Mioni, R., Pavoni, E., Losio, M.N., Sanavio, G. and Croci, L. (2008) Occurrence of enteric viruses in shellfish and relation to climatic-environmental factors. Lett. Appl. Microbiol., 47: 467-474. [Crossref] [PubMed]
11. McLeod, C., Polo, D., Le Saux, J. and Le Guyader, F.S. (2017) Depuration and relaying: A review on potential removal of norovirus from oysters. Comp. Rev. Food Sci. Food Saf., 16: 692-706. [Crossref]
13. Mohan, V., Rawat, S., Lokesh, K.M., Mohan, H.V., Reddy, D.A., Kumar, A. and Bhilegaonkar, K.N. (2014) Prevalence of rotavirus in shellfish from Southern Kerala. Vet. World, 7: 821-824. [Crossref]
14. Anbazhagi, S. and Kamatchiammal, S. (2010) Contamination of seafood by norovirus in India. Int. J. Virol., 6: 138-149. [Crossref]
15. Le Guyader, F., Dubois, E., Menard, D. and Pommepuy, M. (1994) Detection of hepatitis A virus, rotavirus, and enterovirus in naturally contaminated shellfish and sediment by reverse transcription-semi-nested PCR. Appl. Environ. Microbiol., 60: 3665-3671. [PubMed] [PMC]
16. Leparc, I., Aymard, M. and Fuchs, F. (1994) Acute, chronic and persistent enterovirus and poliovirus infections: Detection of viral genome by semi-nested PCR amplification in culture-negative samples. Mol. Cell Probes., 8(6): 487-495. [Crossref] [PubMed]
17. FDA. (2004) Bacteriological Analytical Manual. US Food and Drug Administration Center for Food Safety, Washington, DC.
18. Thebault, A., Teunis, P.F.M., Le Pendu, J., Le Guyader, F.S. and Denis, J.B. (2013) Infectivity of GI and GII noroviruses established from oyster related outbreaks. Epidemics, 5: 98-110. [Crossref] [PubMed]
20. Le Guyader, F., Haugarreau, L., Miossec, L., Dubois, E. and Pommepuy, M. (2000) Three-year study to assess human enteric viruses in shellfish. Appl. Environ. Microbiol., 66: 3241-3248. [Crossref] [PubMed] [PMC]
21. Mesquita, J.R., Vaz, J., Cerqueira, S., Castilho, F., Santos, R., Monteiro, S., Manso, F.C., Romalde, J.L. and Nascimento, M.S.J. (2011) Norovirus, hepatitis A virus and enterovirus presence in shellfish from high-quality harvesting areas in Portugal. Food Microbiol., 28: 936-941. [Crossref] [PubMed]
22. Romalde, J.L., Area, E., Sa'nchez, G., Ribao, C., Torrado, I., Abad, X., Pinto, R.M., Barja, J.L. and Bosch, A. (2002) Prevalence of enterovirus and hepatitis A virus in bivalve molluscs from Galicia (NW Spain): Inadequacy of the EU standards of microbiological quality. Int. J. Food Microbiol., 74: 119-130. [Crossref]
23. Moreno, E., Espigares, E., Mara-on, M., Ma Ochoa, L., Espigares, M. and Fernandez-Crehuet, M. (2014) The prevalence of noroviruses in bivalve molluscs sold in Granada (Spain) fish markets. Molluscan Res., 34: 176-180. [Crossref]
24. Azzouzi, L.M.I., Senouci, S., Qazoui, M.E., Oumzil, H. and Naciri, M. (2017) Detection of enterovirus in mussels from Morocco by cell culture and real-time PCR. Afr. J. Biotechnol., 16: 1791-1799. [Crossref]
25. Noble, R.T. and Fuhrman J.A. (2001) Enteroviruses detected by reverse transcriptase polymerase chain reaction from the coastal waters of Santa Monica Bay, California: Low correlation to bacterial indicator levels. Hydrobiologia, 460: 175-184. [Crossref]
26. Vergara, G.G.R., Goh, S.G., Rezaeinejad, S., Chang, S.Y., Sobsey, M.D. and Gin, K.Y.H. (2015) Evaluation of FRNA coliphages as indicators of human enteric viruses in a tropical urban freshwater catchment. Water Res., 79: 39-47. [Crossref] [PubMed]27. Fong, T.T. and Lipp, E.K. (2005) Enteric viruses of humans and animals in aquatic environments: Health risks, detection, and potential water quality assessment tools. Microbiol. Mol. Biol. Rev., 69(2): 357-371. [Crossref] [PubMed] [PMC]