- Volume 18 Issue 3
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Negative Correlation between the Prevalence of Norovirus and High Bacterial Loads of Escherichia coli in Oysters Crassostrea gigas
Oh, Eun-Gyoung;Song, Ki Cheol;Kim, Sukyung;Park, Kunbawui;Yu, Hongsik
- 투고 : 2015.05.08
- 심사 : 2015.07.13
- 발행 : 2015.09.30
Seasonal variation in the prevalence of norovirus in oysters Crassostrea gigas was investigated and compared to levels of Escherichia coli, a fecal indicator in oysters. Oysters were collected from Iwon-myeon, Taean-gun, Korea, a primary production area for European Union export of oysters between 2013 and 2014. We observed seasonality in the prevalence of norovirus in oysters, with a higher prevalence and viral load detected during winter months. Oysters taken from production areas that complied with the European Union standard for raw consumption (< 230 MPN/100 g of E. coli) had 22.1% of the samples test positive for norovirus (15/68 samples). However, norovirus was not detected in any of the samples (0%, 0/4 samples) that were collected from production sites that exceeded the standard fecal contamination level for raw consumption (> 230 MPN/100 g of E. coli). These results indicated that there is a negative correlation between the prevalence of norovirus and high levels of E. coli in oysters. Therefore, our results suggest that current food safety guidelines using only a bacterial fecal contamination indicator, E. coli, may not adequately assess shellfish production areas for viral and bacterial contamination.
Bivalve molluscs;Oyster;Norovirus;Fecal indicator;Escherichia coli
- Allwood PB, Malik YS, Maherchandani S, Hedberg CW and Goyal SM. 2005. Effect of temperature on the survival of F-specific RNA coliphage, feline calicivirus, and Escherichia coli in chlorinated water. Int J Environ Res Public Health 2, 442-446. https://doi.org/10.3390/ijerph2005030008
- Ang LH. 1998. An outbreak of viral gastroenteritis associated with eating raw oysters. Commun Dis Public Health 1, 38–40.
- Bagordo F, Grassi T, Idolo A, Serio F, Gabutti G and Donno AD. 2013. Rotavirus occurrence in shellfish with low levels of E. coli. Food Environ Virol 5, 169-175. https://doi.org/10.1007/s12560-013-9119-z
- Blanton LH, Adams SM, Beard RS, Wei G, Bulens SN, Widdowson MA, Glass RI and Monroe SS. 2006. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. J Infect Dis 193, 413-421. https://doi.org/10.1086/499315
- Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA and Vinje′ J. 2006. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J Food Prot 69, 2761–2765. https://doi.org/10.4315/0362-028X-69.11.2761
- Carlos JA, Simon RK and Ron JL. 2013 Environmental influences on faecal indicator organisms in coastal waters and their accumulation in bivalve shellfish estuaries and coasts. Est Coast 36, 834-853. https://doi.org/10.1007/s12237-013-9599-y
- Chalmers JWT and McMillan JH. 1995. An outbreak of viral gastroenteritis associated with adequately prepared oysters. Epidemiol Infect 115, 163–167. https://doi.org/10.1017/S0950268800058222
- Clements K, Gimenez L, Jones DL,Wilson J and Malham SK. 2013. Epizoic barnacles act as pathogen reservoirs on shellfish beds. J Shellfish Res 32, 533-538. https://doi.org/10.2983/035.032.0233
- Dancer D, Rangdale RE, Lowther JA and Lees DN. 2010. Human norovirus RNA persists in seawater under simulated winter conditions but does not bioaccumulate efficiently in Pacific oysters (Crassostrea gigas). J Food Prot 73, 2123–2127. https://doi.org/10.4315/0362-028X-73.11.2123
- Diez-Valcarce M, Kokkinos P, Soderberg K, Bouwknegt M, Willems K, de Roda-Husman AM, von Bonsdorff CH, Bellou M, Hernández M, Maunula L, Vantarakis A and Rodriguez-Lazaro D. 2012. Occurrence of human enteric viruses in commercial mussels at retail level in three European countries. Food Environ Virol 4, 73-80. https://doi.org/10.1007/s12560-012-9078-9
- Donia D, Dell'Amico MC, Petrinca AR, Martinucci I, Mazzei M, Tolari F and Diviziaa M. 2012. Presence of hepatitis E RNA in mussels used as bio-monitors of viral marine pollution. J Virol Methods 186, 198-202. https://doi.org/10.1016/j.jviromet.2012.06.007
- Doré WJ, Henshilwood K and Lees DN. 1998. The development of management strategies for control of virological quality in oysters. Water Sci Technol 38, 29–35.
- European Community. 2004. Regulation (EC) no 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. L226. Off J Eur Communities, 83-127.
- Flannery J, Keaveney S and Dore WJ. 2009. Use of FRNA bacteriophages to indicate the risk of norovirus contamination in Irish oysters. J Food Prot 72, 2358-2362. https://doi.org/10.4315/0362-028X-72.11.2358
- Fong TT and Lipp EK. 2005. Enteric viruses of human and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev 69, 357-371. https://doi.org/10.1128/MMBR.69.2.357-371.2005
- Formiga-Cruz M, Tofino-Quesada G, Bofill-Mas S, Lees DN, Henshilwood K, Allard A K, Conden-Hansson AC, Hernroth BE, Vantarakis A, Tsibouxi A, Papapetropoulou M, Furones MD, and Girones R. 2002. Distribution of human virus contamination in shellfish from different growing areas in Greece, Spain, Sweden, and the United Kingdom. Appl Environ Microbiol 68, 5990-5998. https://doi.org/10.1128/AEM.68.12.5990-5998.2002
- Gerba CP, Gramos DM and Nwachuku N. 2002. Comparative inactivation of enterovirus and adenovirus 2 by UV light. Appl Environ Microbiol 68, 5167–5169. https://doi.org/10.1128/AEM.68.10.5167-5169.2002
- Greening GE and Hewitt J. 2008. Norovirus detection in shellfish using a rapid, sensitive virus recovery and real-time RT-PCR detection protocol. Food Analytical Methods 1, 109-118. https://doi.org/10.1007/s12161-008-9018-3
- Greening GE and McCoubrey DJ. 2010. Enteric viruses management of shellfish production in New Zealand. Food Environ Virol 2, 167-175. https://doi.org/10.1007/s12560-010-9041-6
- Haramoto E, Katayama H, Oguma K, Yamashita H, Tajima A, Nakajima H and Ohgaki S. 2006. Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Sci Technol 54, 301-308. https://doi.org/10.2166/wst.2006.888
- International Organization for Standardization. 2005. Microbiology of food and animal feeding stuffs horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli. Part 3. Most probable number technique using 5-bromo-4-chloro-3-indolyl-beta-D-glucuronide. ISO/TS 16649-3. International Organization for Standardization, Geneva, Switzerland
- Jiang S, Noble R and Chu W. 2001. Human adenoviruses and coliphages in urban runoff-impacted coastal waters of Southern California. Appl Environ Microbiol 67, 179-184. https://doi.org/10.1128/AEM.67.1.179-184.2001
- Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N and Katayama K. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clinic Microbiol, 1548-1557.
- KFDA. 2014. Guideline for investigation on the cause of food poisoning. Chapter 5. Korea Food and Drug Administration, ed. Korea Food and Drug Administration, Chungcheonbuk-do, Korea, 182-201.
- 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. https://doi.org/10.1128/AEM.66.8.3241-3248.2000
- Lee HJ, Oh EG, Yu HS, Shin SB, Son MJ, Jung JY, Kim YM and Yoon HD. 2009. Recovery of norovirus surrogate in seawater using an electropositive and electronegative filter. Korean J Fish Aquat Sci 42, 238-242. https://doi.org/10.5657/kfas.2009.42.3.238
- Lees DN. 2000. Viruses in bivalve shellfish. Int J Food Microbiol 59, 81–116. https://doi.org/10.1016/S0168-1605(00)00248-8
- Lees DN. 2010. International standardisation of a method for detection of human pathogenic viruses in molluscan shellfish(CENWG6 TAG4). Food Environ Virol 2, 146 –155.
- Legeay O, Caudrelier Y, Cordevant C, Rigottier-Gois L and Lange M. 2000. Simplified procedure for detection of enteric pathogenic viruses in shellfish by RT-PCR. J Virol Methods 90, 1–14. https://doi.org/10.1016/S0166-0934(00)00174-9
- Lowther JA, Gustar NE, Powell AL, Hartnell RE and Lees DN. 2012. Two-year systematic study to assess norovirus contamination in oysters from commercial harvesting areas in the United Kingdom. Appl Environ Microbiol 78, 5812–5817. https://doi.org/10.1128/AEM.01046-12
- Lowther JA, Henshilwood K and Lees DN. 2008. Determination of norovirus contamination in oysters from two commercial harvesting areas over an extended period, using semiquantitative real-time reverse transcription PCR. J Food Prot 71, 1427-1433. https://doi.org/10.4315/0362-028X-71.7.1427
- Manso CF and Romalde JL. 2013. Detection of hepatitis A virus and norovirus from Galicia (NW Spain). Food Environ Virol 5, 110-118. https://doi.org/10.1007/s12560-013-9108-2
- Shin BS, Oh EG, Yu HS, Son KT, Lee HJ, Park JY and Kim JH. 2013. Genetic Diversity of Noroviruses Detected in Oysters in Jinhae Bay. Korea Food Sci Biotechnol 22, 1453-1460.
- Troussellier M, Bonnefont JL, Courties C, Derrien A, Dupray E, Gauthier M, Gourmelon M, Koux F, Lebaron P, Martin Y and Pommepuy M. 1998. Responses of enteric bacteria to environmental stresses in seawater. Oceanologica Acta 21, 965-981. https://doi.org/10.1016/S0399-1784(99)80019-X
- Influence of Environmental Conditions on Norovirus Presence in Mussels Harvested in Montenegro vol.9, pp.4, 2017, https://doi.org/10.5657/FAS.2015.0235
연구 과제 주관 기관 : National Fisheries Research and Development Institute of Korea