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Detection of Multiple Human Sapoviruses from Imported Frozen Individual Clams

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Abstract

Sapovirus (SaV), a member of the family Caliciviridae, is an important acute gastroenteritis pathogen in humans. Consumption of raw or inadequately cooked clams is one transmission route of human SaV. Sixty individual clams (Ruditapes philippinarum) were from market and tested for human SaVs using two nested reverse transcription-polymerase chain reaction (RT-PCR) assays, one of which was recently developed and effectively detected human SaV from environmental water samples. The nested RT-PCR effective for water samples showed a higher detection rate (68.3 %, 41 of 60 clams) than the other nested RT-PCR (43.3 %, 26 of 60 clams). Based on the sequence analysis of the partial capsid region, SaV strains detected in this study were classified into nine genotypes: GI.1, GI.3, GI.5, GI.6, GI.7, GII.3, GII.4, GIV.1, and GV.1. We demonstrated for the first time the presence of multiple genogroups and/or genotypes of SaV strains in the individual clams. Using a more sensitive assay such as we described to test individual clam samples will help to identify the source of a SaV-gastroenteritis outbreak.

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References

  • Benabbes, L., Ollivier, J., Schaeffer, J., Parnaudeau, S., Rhaissi, H., Nourlil, J., et al. (2012). Norovirus and other human enteric viruses in Moroccan shellfish. Food and Environmental Virology,. doi:10.1007/s12560-012-9095-8.

    Google Scholar 

  • Bon, F., Ambert-Balay, K., Giraudon, H., Kaplon, J., Le Guyader, S., Pommepuy, M., et al. (2005). Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. Journal of Clinical Microbiology, 43(9), 4659–4664.

    Article  PubMed  CAS  Google Scholar 

  • Bucardo, F., Carlsson, B., Nordgren, J., Larson, G., Blandon, P., Vilchez, S., et al. (2012). Susceptibility of children to sapovirus infections, nicaragua, 2005–2006. Emerging Infectious Diseases, 18(11), 1875–1878.

    Article  PubMed  Google Scholar 

  • Green, K. Y. (2007). Caliciviridae. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, & S. E. Straus (Eds.), Fields virology (5th ed., pp. 949–979). Philadelphia: Lippincott Williams & Wilkins.

    Google Scholar 

  • Hansman, G. S., Oka, T., Okamoto, R., Nishida, T., Toda, S., Noda, M., et al. (2007). Human sapovirus in clams, Japan. Emerging Infectious Diseases, 13(4), 620–622.

    Article  PubMed  CAS  Google Scholar 

  • Harada, S., Oka, T., Tokuoka, E., Kiyota, N., Nishimura, K., Shimada, Y., et al. (2012). A confirmation of sapovirus re-infection gastroenteritis cases with different genogroups and genetic shifts in the evolving sapovirus genotypes, 2002–2011. Archives of Virology, 157(10), 1999–2003.

    Article  PubMed  CAS  Google Scholar 

  • Harada, S., Okada, M., Yahiro, S., Nishimura, K., Matsuo, S., Miyasaka, J., et al. (2009). Surveillance of pathogens in outpatients with gastroenteritis and characterization of sapovirus strains between 2002 and 2007 in Kumamoto Prefecture, Japan. Journal of Medical Virology, 81(6), 1117–1127.

    Article  PubMed  Google Scholar 

  • Haramoto, E., Kitajima, M., Kishida, N., Katayama, H., Asami, M., & Akiba, M. (2012). Occurrence of viruses and protozoa in drinking water sources of Japan and their relationship to indicator microorganisms. Food and Environmental Virology, 4(3), 93–101.

    Article  PubMed  Google Scholar 

  • Iizuka, S., Oka, T., Tabara, K., Omura, T., Katayama, K., Takeda, N., et al. (2010). Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish. Journal of Medical Virology, 82(7), 1247–1254.

    Article  PubMed  Google Scholar 

  • Iwai, M., Hasegawa, S., Obara, M., Nakamura, K., Horimoto, E., Takizawa, T., et al. (2009). Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Applied and Environmental Microbiology, 75(5), 1264–1270.

    Article  PubMed  CAS  Google Scholar 

  • Johansson, P. J., Bergentoft, K., Larsson, P. A., Magnusson, G., Widell, A., Thorhagen, M., et al. (2005). A nosocomial sapovirus-associated outbreak of gastroenteritis in adults. Scandinavian Journal of Infectious Diseases, 37(3), 200–204.

    Article  PubMed  Google Scholar 

  • Kitajima, M., Haramoto, E., Phanuwan, C., & Katayama, H. (2011). Genotype distribution of human sapoviruses in wastewater in Japan. Applied and Environmental Microbiology, 77(12), 4226–4229.

    Article  PubMed  Google Scholar 

  • Kitajima, M., Oka, T., Haramoto, E., Katayama, H., Takeda, N., Katayama, K., et al. (2010). Detection and genetic analysis of human sapoviruses in river water in Japan. Applied and Environmental Microbiology, 76(8), 2461–2467.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, S., Fujiwara, N., Yasui, Y., Yamashita, T., Hiramatsu, R., & Minagawa, H. (2012). A foodborne outbreak of sapovirus linked to catered box lunches in Japan. Archives of Virology, 157(10), 1995–1997.

    Article  PubMed  CAS  Google Scholar 

  • Le Guyader, F. S., Krol, J., Ambert-Balay, K., Ruvoen-Clouet, N., Desaubliaux, B., Parnaudeau, S., et al. (2010). Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. Journal of Clinical Microbiology, 48(3), 915–920.

    Article  PubMed  Google Scholar 

  • Lee, L. E., Cebelinski, E. A., Fuller, C., Keene, W. E., Smith, K., Vinje, J., et al. (2012). Sapovirus outbreaks in long-term care facilities, Oregon and Minnesota, USA, 2002–2009. Emerging Infectious Diseases, 18(5), 873–876.

    Article  PubMed  Google Scholar 

  • Medici, M. C., Tummolo, F., Albonetti, V., Abelli, L. A., Chezzi, C., & Calderaro, A. (2012). Molecular detection and epidemiology of astrovirus, bocavirus, and sapovirus in Italian children admitted to hospital with acute gastroenteritis, 2008–2009. Journal of Medical Virology, 84(4), 643–650.

    Article  PubMed  Google Scholar 

  • Nakagawa-Okamoto, R., Arita-Nishida, T., Toda, S., Kato, H., Iwata, H., Akiyama, M., et al. (2009). Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks. Japanese Journal of Infectious Diseases, 62(1), 63–66.

    PubMed  CAS  Google Scholar 

  • Noel, J. S., Liu, B. L., Humphrey, C. D., Rodriguez, E. M., Lambden, P. R., Clarke, I. N., et al. (1997). Parkville virus: a novel genetic variant of human calicivirus in the Sapporo virus clade, associated with an outbreak of gastroenteritis in adults. Journal of Medical Virology, 52(2), 173–178.

    Article  PubMed  CAS  Google Scholar 

  • Oka, T., Mori, K., Iritani, N., Harada, S., Ueki, Y., Iizuka, S., et al. (2012). Human sapovirus classification based on complete capsid nucleotide sequences. Archives of Virology, 157(2), 349–352.

    Article  PubMed  CAS  Google Scholar 

  • Okada, M., Yamashita, Y., Oseto, M., & Shinozaki, K. (2006). The detection of human sapoviruses with universal and genogroup-specific primers. Archives of Virology, 151(12), 2503–2509.

    Article  PubMed  CAS  Google Scholar 

  • Pang, X. L., Lee, B. E., Tyrrell, G. J., & Preiksaitis, J. K. (2009). Epidemiology and genotype analysis of sapovirus associated with gastroenteritis outbreaks in Alberta, Canada: 2004–2007. The Journal of Infectious Diseases, 199(4), 547–551.

    Article  PubMed  Google Scholar 

  • Perriere, G., & Gouy, M. (1996). WWW-query: an on-line retrieval system for biological sequence banks. Biochimie, 78(5), 364–369.

    Article  PubMed  CAS  Google Scholar 

  • Sano, D., Perez-Sautu, U., Guix, S., Pinto, R. M., Miura, T., Okabe, S., et al. (2011). Quantification and genotyping of human sapoviruses in the Llobregat river catchment, Spain. Applied and Environmental Microbiology, 77(3), 1111–1114.

    Article  PubMed  CAS  Google Scholar 

  • Svraka, S., Vennema, H., van der Veer, B., Hedlund, K. O., Thorhagen, M., Siebenga, J., et al. (2010). Epidemiology and genotype analysis of emerging sapovirus-associated infections across Europe. Journal of Clinical Microbiology, 48(6), 2191–2198.

    Article  PubMed  CAS  Google Scholar 

  • Ueki, Y., Shoji, M., Okimura, Y., Miyota, Y., Masago, Y., Oka, T., et al. (2010). Detection of sapovirus in oysters. Microbiology and Immunology, 54(8), 483–486.

    Article  PubMed  CAS  Google Scholar 

  • Usuku, S., Kumazaki, M., Kitamura, K., Tochikubo, O., & Noguchi, Y. (2008). An outbreak of food-borne gastroenteritis due to sapovirus among junior high school students. Japanese Journal of Infectious Diseases, 61(6), 438–441.

    PubMed  Google Scholar 

  • Yamashita, Y., Ootsuka, Y., Kondo, R., Oseto, M., Doi, M., Miyamoto, T., et al. (2010). Molecular characterization of sapovirus detected in a gastroenteritis outbreak at a wedding hall. Journal of Medical Virology, 82(4), 720–726.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida, T., Kasuo, S., Azegami, Y., Uchiyama, Y., Satsumabayashi, K., Shiraishi, T., et al. (2009). Characterization of sapoviruses detected in gastroenteritis outbreaks and identification of asymptomatic adults with high viral load. Journal of Clinical Virology, 45(1), 67–71.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by a Grant-in-Aid for Food safety from the Ministry of Health, Labour, and Welfare, Japan.

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Correspondence to Tomoichiro Oka.

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Setsuko Iizuka and Reiko Takai-Todaka contributed equally to this study.

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Iizuka, S., Takai-Todaka, R., Ohshiro, H. et al. Detection of Multiple Human Sapoviruses from Imported Frozen Individual Clams. Food Environ Virol 5, 119–125 (2013). https://doi.org/10.1007/s12560-013-9109-1

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  • DOI: https://doi.org/10.1007/s12560-013-9109-1

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