Abstract
The potential of high pressure processing to inactivate hepatitis A virus (HAV) within Mediterranean mussels (Mytilus galloprovincialis) and blue mussels (Mytilus edulis) was evaluated. HAV was bioaccumulated within mussels to approximately 6-log10 PFU by exposure of mussels to HAV-contaminated seawater. After shucking, 5 min pressure treatments of 300, 325, 350, 375, and 400 MegaPascals (MPa) were performed at room temperature (18–22°C). For blue mussels, log10 PFU reductions of HAV averaged 2.1 and 3.6 for treatments of 350 and 400 MPa, while for Mediterranean mussels reductions of 1.7 and 2.9 log10 PFU MPa were observed for equivalent treatments. These results demonstrate that high pressure processing is capable of inactivating HAV within mussels.
Similar content being viewed by others
References
Ajelli, M., Iannelli, M., Manfredi, P., & degli Atti, M. L. (2008). Basic mathematical models for the temporal dynamics of HAV in medium-endemicity Italian areas. Vaccine, 26, 1697–1707.
Berlin, D. L., Herson, D. S., Hicks, D. T., & Hoover, D. G. (1999). Response of pathogenic Vibrio species to high hydrostatic pressure. Applied and Environmental Microbiology, 65, 2776–2780.
Bosch, A., Pintó, R. M., & Abad, F. X. (1995). Differential accumulation and depuration of human enteric viruses by mussels. Water Science and Technology, 31, 447–451.
Calci, K. R., Burkhardt, W., & Smith, A. V. (2002). High hydrostatic pressure inactivation of calicivirus (SMSV-17) in oysters. International Association for Food Protection Annual Meeting, San Diego, CA, June 30–July 3 Abstract #P224.
Calci, K. R., Meade, G. K., Tetzloff, R. C., & Kingsley, D. H. (2005). High-pressure inactivation of hepatitis A virus within oysters. Applied and Environmental Microbiology, 71, 339–343.
Chen, H., Hoover, D. G., & Kingsley, D. H. (2005). Temperature and treatment time influence high hydrostatic pressure inactivation of feline calicivirus, a norovirus surrogate. Journal of Food Protection, 68, 2389–2394.
Chironna, M., Germinaro, C., DeMedici, D., Fiore, A., DiPasquale, S., Quarto, M., et al. (2002). Detection of hepatitis A virus in mussels from different sources marketed in Puglia region (South Italy). International Journal of Food Microbiology, 75, 11–18.
Cliver, D. O. (1997). Virus transmission via food. Food Technology, 51, 71–78.
Cook, D. W. (2003). Sensitivity of Vibrio species in phosphate buffered saline and in oysters to high pressure processing. Journal of Food Protection, 66, 2276–8266.
Costafreida, M. I., Bosch, A., & Pintó, R. M. (2006). Development, evaluation, and standardization of a real-time reverse-transcription PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Applied and Environmental Microbiology, 72, 3846–3855.
Croci, L., De Medici, D., Morace, G., Fiore, A., Scalfaro, C., Beneduce, F., et al. (1999). Detection of hepatitis A virus in shellfish by nested reverse transcription-PCR. International Journal of Food Microbiology, 48, 67–71.
Croci, L., DeMedici, D., DiPaquale, S., & Toti, L. (2005). Resistance of hepatitis A virus in mussels subjected to different domestic cookings. International Journal of Food Microbiology, 105, 139–144.
Croci, L., Losio, M. N., Suffredini, E., DiPasquale, S., Fallacara, F., & Arcangeli, G. (2007). Assessment of human enteric viruses in shellfish from the northern Adriatic sea. International Journal of Food Microbiology, 114, 252–257.
Cromeans, T., Sobsey, M. D., & Fields, H. A. (1987). Development of a plaque assay for a cytopathic, rapidly replicating isolate of hepatitis A virus. Journal of Medical Virology, 22, 45–56.
De Medici, D., Ciccozzi, M., Fiore, A., Di Pasquale, S., Parlato, A., Ricci-Bitti, P., et al. (2001). Closed-circuit system for the depuration of mussels experimentally contaminated with hepatitis A virus. Journal of Food Protection, 64, 877–880.
Di Pinto, A., Forte, V. T., Tantillo, G. M., Terio, V., & Buonavoglia, C. (2003). Detection of hepatitis A virus in shellfish (Mytilus galloprovincialis) with RT-PCR. Journal of Food Protection, 66, 1681–1685.
Enriquez, R., Frösner, G. G., Hochstein-Mintzel, V., Riedemann, S., & Reinhardt, G. (1992). Accumulation and persistence of hepatitis A virus in mussels. Journal of Medical Virology, 37, 174–179.
FitzSimons, D., Hendrickx, G., Vorsters, A., & Van Damme, P. (2010). Hepatitis A and E: Update on prevention and epidemiology. Vaccine, 28, 583–588.
Franco, E., Toti, L., Gabrieli, R., Croci, L., Demedici, D., & Pana, A. (1990). Depuration of Mytilis galloprovincialis experimentally contaminated with hepatitis A virus. International Journal of Food Microbiology, 11, 321–327.
Grove, S. F., Lee, A., Stewart, C. M., & Ross, T. (2009). Development of a high pressure processing inactivation model for hepatitis A virus. Journal of Food Protection, 72, 1434–1442.
He, H., Adams, R. M., Farkas, D. F., & Morrissey, M. T. (2002). Use of high-pressure processing for oyster shucking and shelf-life extension. Journal of Food Science, 67, 640–645.
Kingsley, D. H., Calci, K., Holliman, S., Dancho, B., & Flick, G. J. (2009). High pressure inactivation of HAV within oysters: Comparison of whole-in-shell with shucked oyster meats. Food and Environmental Virology, 1, 137–140.
Kingsley, D. H., & Chen, H. (2008). Aqueous matrix composition influences feline calicivirus inactivation by high pressure processing. Journal of Food Protection, 71, 1598–1603.
Kingsley, D. H., & Chen, H. (2009). Influence of pH, salt, and temperature on pressure inactivation of hepatitis A virus. International Journal of Food Microbiology, 130, 61–64.
Kingsley, D. H., Guan, D. S., & Hoover, D. G. (2005). Pressure inactivation of hepatitis A virus in strawberry puree and sliced green onions. Journal of Food Protection, 68, 1748–1751.
Kingsley, D. H., Guan, D., Hoover, D. G., & Chen, H. (2006). Inactivation of hepatitis A virus by high pressure processing: The role of temperature and pressure oscillation. Journal of Food Protection, 69, 2454–2459.
Kingsley, D. H., Holliman, D. R., Calci, K. R., Chen, H., & Flick, G. J. (2007). Inactivation of a norovirus by high pressure processing. Applied and Environmental Microbiology, 73, 581–585.
Kingsley, D. H., Hoover, D., Papafragkou, E., & Richards, G. P. (2002). Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. Journal of Food Protection, 65, 1605–1609.
Kingsley, D. H., & Richards, G. P. (2003). Persistence of hepatitis A virus within oysters. Journal of Food Protection, 66, 331–334.
Kural, A. G., & Chen, H. Q. (2008). Conditions for a 5-log reduction of Vibrio vulnificus in oysters through high hydrostatic pressure treatment. International Journal of Food Microbiology, 122, 180–187.
Kural, A. G., Shearer, A. E. H., Kingsley, D. H., & Chen, H. (2008). Conditions for high pressure inactivation of Vibrio parahaemolyticus in oysters. International Journal of Food Microbiology, 127, 1–5.
Lopez-Caballero, M. E., Perez-Mateos, M., Montero, P., & Borderias, A. J. (2000). Oyster preservation by high-pressure treatment. Journal of Food Protection, 63, 196–201.
Macaluso, A., Petrinca, A., Lanni, L., Saccares, S., Amiti, S., Gabrieli, R., et al. (2006). Identification and sequence analysis of hepatitis A virus in market and environment bivalve mollusks. Journal of Food Protection, 69, 449–452.
McLeod, C., Hay, B., Grant, C., Greening, G., & Day, D. (2009). Inactivation and elimination of human enteric viruses by Pacific oysters. Journal of Applied Microbiology, 107, 1809–1818.
Pintó, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish outbreaks of hepatitis A. Applied and Environmental Microbiology, 75, 7350–7355.
Pontrelli, G., Boccia, D., Di Renzi, M., Massari, M., Giugliano, F., Clentano, L. P., et al. (2008). Epidemiological and virological characterization of a large community-wide outbreak of hepatitis A in southern Italy. Epidemiology and Infection, 136, 1027–1034.
Richards, G. P. (1988). Microbial purification of shellfish: A review of depuration and relaying. Journal of Food Protection, 51, 218–251.
Richards, G. P., & Watson, M. A. (2001). Immunochemiluminescent focus assays for the quantitation of hepatitis A virus and rotavirus in cell cultures. Journal of Virological Methods, 94, 69–80.
Romalde, J. L., Area, E., Sánchez, G., Ribao, C., Torrado, I., Abad, X., et al. (2002). Prevalence of enterovirus and hepatitis A virus in bivalve mollusks from Galicia (NW Spain): Inadequacy of the EU standards of microbiological quality. International Journal of Food Microbiology, 74, 119–130.
Romalde, J. L., Torrado, I., Ribao, C., & Barja, J. L. (2001). Global market: Shellfish imports as a source of reemerging food-borne hepatitis A virus infections in Spain. International Microbiology, 4, 223–226.
Sanchez, G., Pintó, R. M., Vanaclocha, H., & Bosch, A. (2002). Molecular characterization of hepatitis A virus isolates from a transcontinental shellfish-borne outbreak. Journal of Clinical Microbiology, 40, 4148–4155.
Shieh, Y. C., Khudyakov, Y. E., Xia, G., Ganova-Raeva, L. M., Khambaty, F. M., Woods, J. W., et al. (2007). Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multistate outbreak. Journal of Food Protection, 70, 145–150.
Shimasaki, N., Kiyohara, T., Totsuka, A., Nojima, K., Okada, Y., Yamaguchi, K., et al. (2009). Inactivation of hepatitis A virus by heat and high hydrostatic pressure: Variation among laboratory strains. Vox Sanguinis, 96, 14–19.
Suffredini, E., Corrain, C., Arcangeli, G., Fasolato, L., Manfrin, A., Rossetti, E., et al. (2008). Occurrence of enteric viruses in shellfish and relation to climatic-environmental factors. Letters in Applied Microbiology, 47, 467–474.
Acknowledgments
We wish to thank Gloria Meade (USDA, Dover DE) and Valeriana Colao (University of Bari) for technical assistance. We also wish to thank Gary Richards (USDA, Dover, DE, USA) and Pina Fratamico (USDA, Wyndmoor, PA, USA) for critical review of the manuscript.
Disclaimer
Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Terio, V., Tantillo, G., Martella, V. et al. High Pressure Inactivation of HAV Within Mussels. Food Environ Virol 2, 83–88 (2010). https://doi.org/10.1007/s12560-010-9032-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-010-9032-7