Detection and genetic characterization of human enteric viruses in oyster-associated gastroenteritis outbreaks between 2001 and 2012 in Osaka City, Japan

Journal of Medical Virology

Volumn 86, Issue 12, 2014, Pages 2019-2025

  Iritani, Nobuhiro ^a   Kaida, Atsushi ^a   Abe, Niichiro ^a   Kubo, Hideyuki ^a   Sekiguchi, Jun Ichiro ^a   Yamamoto, Seiji P ^a   Goto, Kaoru ^a   Tanaka, Tomoyuki ^b   Noda, Mamoru ^c  

^a OSAKA CITY INSTITUTE OF PUBLIC HEALTH AND ENVIRONMENTAL SCIENCES   (Japan)

^b Sakai City Institute of Public Health   (Japan)

^c NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Aichivirus; Astrovirus; Enterovirus; Norovirus; Sapovirus

Indexed keywords

VIRUS DNA; VIRUS RNA;

ADULT; AICHIVIRUS; ARTICLE; ASTROVIRUS; ASTROVIRUS INFECTION; ENTERIC VIRUS; FOOD CONTAMINATION; FOOD INTAKE; HUMAN; MAJOR CLINICAL STUDY; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; OYSTER; PHYLOGENY; PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS A; SAPOVIRUS; SHELLFISH; VIRAL GASTROENTERITIS; VIRUS DETECTION; VIRUS TRANSMISSION; ADOLESCENT; AGED; ANIMAL; CLASSIFICATION; DNA SEQUENCE; EPIDEMIC; FECES; FEMALE; FOODBORNE DISEASES; GASTROENTERITIS; GENETICS; ISOLATION AND PURIFICATION; JAPAN; MALE; MIDDLE AGED; MOLECULAR GENETICS; VERY ELDERLY; VIROLOGY; VIRUS; YOUNG ADULT;

ASTROVIRIDAE; ENTEROVIRUS; NOROVIRUS; OSTREIDAE; SAPOVIRUS;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; DISEASE OUTBREAKS; FECES; FEMALE; FOODBORNE DISEASES; GASTROENTERITIS; HUMANS; JAPAN; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; OSTREIDAE; SEQUENCE ANALYSIS, DNA; VIRUSES; YOUNG ADULT;

EID: 84911808345     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23883     Document Type: Article

References (49)

1. Alfano-Sobsey E, Sweat D, Hall A, Breedlove F, Rodriguez R, Greene S, Pierce A, Sobsey M, Davies M, Ledford SL. 2012. Norovirus outbreak associated with undercooked oysters and secondary household transmission. Epidemiol Infect 140:276-282.
2. Begier EM, Oberste MS, Landry ML, Brennan T, Mlynarski D, Mshar PA, Frenette K, Rabatsky-Ehr T, Purviance K, Nepaul A, Nix WA, Pallansch MA, Ferguson D, Cartter ML, Hadler JL. 2008. An outbreak of concurrent echovirus 30 and coxsackievirus A1 infections associated with sea swimming among a group of travelers to Mexico. Clin Infect Dis 47:616-623.
3. Benabbes L, Ollivier J, Schaeffer J, Parnaudeau S, Rhaissi H, Nourlil J, Le Guyader FS. 2013. Norovirus and other human enteric viruses in Moroccan shellfish. Food Environ Virol 5:35-40.
4. Chitambar S, Gopalkrishna V, Chhabra P, Patil P, Verma H, Lahon A, Arora R, Tatte V, Ranshing S, Dhale G, Kolhapure R, Tikute S, Kulkarni J, Bhardwaj R, Akarte S, Pawar S. 2012. Diversity in the enteric viruses detected in outbreaks of gastroenteritis from Mumbai, Western India. Int J Environ Res Public Health 9:895-915.
5. Choo YJ, Kim SJ. 2006. Detection of human adenoviruses and enteroviruses in Korean oysters using cell culture, integrated cell culture-PCR, and direct PCR. J Microbiol 44:162-170.
6. Christensen BF, Lees D, Henshilwood K, Bjergskov T, Green J. 1998. Human enteric viruses in oysters causing a large outbreak of human food borne infection in 1996/97. J Shellfish Res 17:1633-1635.
7. Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.
8. Hansman GS, Oka T, Katayama K, Takeda N. 2007. Human sapoviruses: Genetic diversity, recombination, and classification. Rev Med Virol 17:133-141.
9. Hansman GS, Oka T, Li TC, Nishio O, Noda M, Takeda N. 2008. Detection of human enteric viruses in Japanese clams. J Food Prot 71:1689-1695.
10. Iizuka S, Oka T, Tabara K, Omura T, Katayama K, Takeda N, Noda M. 2010. Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish. J Med Virol 82:1247-1254.
11. Iritani N, Seto Y, Haruki K, Kimura M, Ayata M, Ogura H. 2000. Major change in the predominant type of "Norwalk-like viruses" in outbreaks of acute nonbacterial gastroenteritis in Osaka City, Japan, between April 1996 and March 1999. J Clin Microbiol 38:2649-2654.
12. Iritani N, Seto Y, Kubo H, Haruki K, Ayata M, Ogura H. 2002. Prevalence of "Norwalk-like virus" infections in outbreaks of acute nonbacterial gastroenteritis observed during the 1999-2000 season in Osaka City, Japan. J Med Virol 66:131-138.
13. Iritani N, Kaida A, Kubo H, Abe N, Murakami T, Vennema H, Koopmans M, Takeda N, Ogura H, Seto Y. 2008. Epidemic of genotype GII.2 noroviruses during 2004 in Osaka City, Japan. J Clin Microbiol 46:2406-2409.
14. Iritani N, Kaida A, Kubo H, Abe N, Goto K, Ogura H, Seto Y. 2010. Molecular epidemiology of noroviruses detected in seasonal outbreaks of acute nonbacterial gastroenteritis in Osaka City, Japan, from 1996-1997 to 2008-2009. J Med Virol 82:2097-2105.
15. Iritani N, Kaida A, Abe N, Sekiguchi J, Kubo H, Takakura K, Goto K, Ogura H, Seto Y. 2012. Increase of GII.2 norovirus infections during the 2009-2010 season in Osaka City, Japan. J Med Virol 84:517-525.
16. Ito M, Yamashita T, Tsuzuki H, Takeda N, Sakae K. 2004. Isolation and identification of a novel human parechovirus. J Gen Virol 85:391-398.
17. Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41:1548-1557.
18. Kaida A, Kubo H, Takakura K, Iritani N. 2010. Detection of quantitative analysis of human bocavirus associated with respiratory tract infection in Osaka City, Japan. Microbiol Immunol 54:276-281.
19. Kaida A, Kubo H, Takakura K, Sekiguchi J, Yamamoto SP, Kohdera U, Togawa M, Amo K, Shiomi M, Ohyama M, Goto K, Hase A, Kageyama T, Iritani N. Mutual association of co-infected respiratory viruses in children with acute respiratory tract infections (under review).
20. Kantola K, Sadeghi M, Antikainen J, Kirverskari J, Delwart E, Hedman K, Soderlund-Venermo M. 2010. Real-time quantitative PCR detection of four human bocaviruses. J Clin Microbiol 48:4044-4050.
21. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120.
22. Koopmans M, Duizer E. 2004. Foodborne viruses: An emerging problem. Int J Food Microbiol 90:23-41.
23. Koopmans M, von Bonsdorff CH, Vinjé J, de Medici D, Monroe S. 2002. Foodborne viruses. FEMS Microbiol Rev 26:187-205.
24. Kroneman A, Vennema H, Deforche K, van der Avoort H, Peñaranda S, Oberste MS, Vinjé J, Koopmans M. 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51:121-125.
25. Kuzuya M, Fujii R, Hamano M, Nakamura J, Yamada M, Nii S, Mori T. 1996. Molecular analysis of outer capsid glycoprotein (VP7) genes from two isolates of human group C rotavirus with different genome electropherotypes. J Clin Microbiol 34:3185-3189.
26. Le Guyader FS, Haugarreau L, Miossec L, Dubois E, Pmmepuy M. 2000. Three-year study to assess human enteric viruses in Shellfish. Appl Environ Microbiol 66:3241-3248.
27. Le Guyader FS, Bon F, DeMedici D, Parnaudeau S, Bertone A, Crudeli S, Doyle A, Zidane M, Suffredini E, Kohli E, Maddalo F, Monini M, Gallay A, Pommepuy M, Pothier P, Ruggeri FM. 2006. Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. J Clin Microbiol 44:3878-3882.
28. Le Guyader FS, Le Saux JC, Ambert-Balay K, Krol J, Serais O, Parnaudeau S, Giraudon H, Delmas G, Pommepuy M, Pothier P, Atmar RL. 2008. Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. J Clin Microbiol 46:4011-4017.
29. Liu LJ, Liu W, Liu YX, Xiao HJ, Jia N, Liu G, Tong YG, Cao WC. 2010. Identification of norovirus as the top enteric viruses detected in adult cases with acute gastroenteritis. Am J Trop Med Hyg 82:717-722.
30. Nakagawa-Okamoto R, Arita-Nishida T, Toda S, Kato H, Iwata H, Akiyama M, Nishio O, Kimura H, Noda M, Takeda N, Oka T. 2009. Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks. Jpn J Infect Dis 62:63-66.
31. Nix WA, Oberste MS, Pallansch MA. 2006. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 44:2698-2704.
32. Oberste MS, Maher K, Michele SM, Belliot G, Uddin M, Pallansch MA. 2005. Enteroviruses 76, 89, 90 and 91 represent a novel group within the species Human enterovirus A. J Gen Virol 86:445-451.
33. Oka T, Katayama K, Hansman GS, Kageyama T, Ogawa S, Wu FT, White PA, Takeda N. 2006. Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. J Med Virol 78:1347-1353.
34. Oka T, Mori K, Iritani N, Harada S, Ueki Y, Iizuka S, Mise K, Murakami K, Wakita T, Katayama K. 2012. Human sapovirus classification based on complete capsid nucleotide sequences. Arch Virol 157:349-352.
35. Okada M, Yamashita Y, Oseto M, Shinozaki K. 2006. The detection of human sapoviruses with universal and genogroup-specific primers. Arch Virol 151:2503-2509.
36. Pager CT, Steele AD. 2002. Astrovirus-associated diarrhea in South African adults. Clin Infect Dis 35:1451-1452.
37. Pang XL, Lee BE, Tyrrell GJ, Preiksaitis JK. 2009. Epidemiology and genotype analysis of sapovirus associated with gastroenteritis outbreaks in Alberta, Canada: 2004-2007. J Infect Dis 199:547-551.
38. Prato R, Lopalco PL, Chironna M, Barbuti G, Germinario C, Quarto M. 2004. Norovirus gastroenteritis general outbreak associated with raw shellfish consumption in South Italy. BMC Infect Dis 4:37.
39. Sakon N, Yamazaki K, Utagawa E, Okuno Y, Oishi I. 2000. Genomic characterization of human astrovirus type 6 Katano virus and the establishment of a rapid and effective reverse transcription-polymerase chain reaction to detect all serotypes of human astrovirus. J Med Virol 61:125-131.
40. Seymour IJ, Appleton H. 2001. Foodborne viruses and fresh produce. J Appl Microbiol 91:759-773.
41. Shieh YC, Monroe SS, Fankhauser RL, Langlois GW, Burkhardt W III, Baric RS. 2000. Detection of Norwalk-like virus in shellfish implicated in illness. J Infect Dis 181:S360-S366.
42. Svraka S, Vennema H, van der Veer B, Hedlund KO, Thorhangen M, Siebenga J, Duizer E, Koopmans M. 2010. Epidemiology and genotype analysis of emerging sapovirus-associated infections across Europe. J Clin Microbiol 48:2191-2198.
43. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The Clustal X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
44. Ueki Y, Shoji M, Okimura Y, Miyota Y, Masago Y, Oka T, Katayama K, Takeda N, Noda M, Miura T, Sano D, Omura T. 2010. Detection of sapovirus in oysters. Microbiol Immunol 54:483-486.
45. Umesha KR, Bhavani NC, Venugopal MN, Karunasagar I, Krohne G, Karunasagar I. 2008. Prevalence of human pathogenic enteric viruses in bivalve molluscan shellfish and cultured shrimp in south coast of India. Int J Food Microbiol 122:279-286.
46. Walter JE, Mitchell DK. 2003. Astrovirus infection in children. Curr Opin Infect Dis 16:247-253.
47. Webby RJ, Carville KS, Kirk MD, Greening G, Ratcliff RM, Crerar SK, Dempsey K, Sarna M, Stafford R, Patel M, Hall G. 2007. Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clin Infect Dis 44:1026-1031.
48. Westrell T, Dusch V, Ethelberg S, Harris J, Hjertqvist M, Jourdan-da Silva N, Koller A, Lenglet A, Lisby M, Vold L. 2010. Norovirus outbreaks linked to oyster consumption in the United Kingdom, Norway, France, Sweden and Penmark, 2010. Euro Surveill 15: pii=19524. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19524
49. Yamashita T, Sugiyama M, Tsuzuki H, Sakae K, Suzuki Y, Miyazaki Y. 2000. Application of a reverse transcription-PCR for identification and differentiation of aichi virus, a new member of the picornavirus family associated with gastroenteritis in human. J Clin Microbiol 38:2955-2961.