Seroprevalence of Norovirus Genogroup IV Antibodies among Humans, Italy, 2010–2011 - Volume 20, Number 11—November 2014 - Emerging Infectious Disease journal - CDC
Volume 20, Number 11—November 2014
Seroprevalence of Norovirus Genogroup IV Antibodies among Humans, Italy, 2010–2011
Noroviruses (NoVs) are a major cause of epidemic gastroenteritis in children and adults. They cause nearly half of all gastroenteritis cases and >90% of nonbacterial gastroenteritis epidemics worldwide (1). NoVs belong to the genus Norovirus in the family Caliciviridae (2,3). NoV virions are nonenveloped and ≈30 to 35 nm in diameter. The icosahedral capsid surrounds a 7.7-kb positive-sense single-stranded RNA genome covalently linked to viral protein g (VPg) at the 5′ end and polyadenylated at the 3′ end (4). The RNA genome is organized into 3 open reading frames (ORFs). ORF1 encodes a polyprotein that is cleaved by the virus-encoded protease to produce several nonstructural proteins, including the RNA-dependent RNA polymerase; ORF2 encodes a major capsid protein, VP1; and ORF3 encodes a small basic protein (VP2) that has been associated with the stability of the capsid (4,5). Based on the full-length VP1 aa sequence, NoVs have been divided into 6 genogroups (GI to GVI) and multiple genotypes (6,7). However, only GI, GII, and GIV NoVs have been shown to infect humans; GII strains are the most prevalent worldwide (4). Human GIV NoV (Alphatron-like) strains have been identified at low prevalence from either sporadic cases or outbreaks of human gastroenteritis (8–10). However, analysis of wastewater, sewage, and seafood in Japan and Italy has revealed, indirectly, that GIV NoVs are common in humans (11–14).
GIV.2 NoVs (strain GIV.2/Pistoia/387/06/ITA) were first detected in the feces of a captive lion cub with severe hemorrhagic enteritis in Italy (15). Subsequently, similar NoVs were identified in fecal samples of dogs and cats with diarrhea (16,17). Sequence comparison in the VP1 of human and animal GIV NoVs has revealed that, although they are genetically related, the 2 groups of viruses represent 2 distinct genotypes: GIV.1 viruses predominate in humans and GIV.2 in animals (7,15). Historical evidence shows that viruses genetically and antigenically closely related to human NoVs might infect animals (15–19). Also, a human GII.4 NoV strain has been found to replicate and cause clinical signs and lesions in experimentally-infected gnotobiotic pigs and calves (20,21). These findings have raised public health concerns about potential cross-species transmission and generation of novel human NoV strains by recombination. The close genetic relatedness (17,22) of human and animal GIV NoVs indicates that they may have originated from a common ancestor. Interspecies transmission between humans and pets might have been facilitated by the social interactions established since domestication of small carnivores. This eventuality has been demonstrated firmly in a recent study in Finland, which reported the detection of GII.4 and GII.12 NoVs in the dogs belonging to human patients hospitalized with NoV gastroenteritis (19). To address whether cross-species transmission of GIV.2 might occur between carnivores and humans, we investigated the prevalence of antibodies against GIV.1 and GIV.2 NoVs in a representative population in Italy spanning all age groups.
Dr Di Martino is a researcher at the Faculty of Veterinary Medicine of Teramo, Italy. Her research interests include the study of human and animal noroviruses, with particular emphasis on development of recombinant diagnostic tools.
This study was supported by grants from the University of Teramo, Italy, and from the Italian Ministry of University and Research, and was also partially funded by the intramural research program of the National Institute of Infectious Diseases, National Institutes of Health, US.
- Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinjé J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis.Emerg Infect Dis. 2008;14:1224–31 .
- Green J, Vinje J, Gallimore CI, Koopmans M, Hale A, Brown DW, Capsid protein diversity among Norwalk-like viruses. Virus Genes. 2000;20:227–36.
- Carstens EB. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch Virol.2010;155:133–46.
- Green KY. Caliciviridae: The noroviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, et al., editors. Fields virology, 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2007. p. 949–79.
- Bertolotti-Ciarlet A, Crawford SE, Hutson AM, Estes MK. The 3′ end of Norwalk virus mRNA contains determinants that regulate the expression and stability of the viral capsid protein VP1: a novel function for the VP2 protein. J Virol. 2003;77:11603–15.
- Martella V, Decaro N, Lorusso E, Radogna A, Moschidou P, Amorisco F, Genetic heterogeneity and recombination in canine noroviruses. J Virol.2009;83:11391–6.
- Zheng DP, Ando T, Frankhouser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology.2006;346:312–23.
- Vinjé J, Koopmans MP. Simultaneous detection and genotyping of “Norwalk-like viruses” by oligonucleotide array in a reverse line blot hybridization format. J Clin Microbiol. 2000;38:2595–601 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC86977/.
- Iritani N, Seto Y, Kubo H, Haruki K, Ayata M, Ogura H. 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. 2002;66:131–8.
- La Rosa G, Pourshaban M, Iaconelli M, Muscillo M. Detection of genogroup IV noroviruses in environmental and clinical samples and partial sequencing through rapid amplification of cDNA ends. Arch Virol. 2008;153:2077–83.
- Kitajima M, Haramoto E, Phanuwan C, Katayama H, Ohgaki S. Detection of genogroup IV norovirus in wastewater and river water in Japan. Lett Appl Microbiol. 2009;49:655–8.
- La Rosa G, Iaconelli M, Pourshaban M, Fratini M, Muscillo M. Molecular detection and genetic diversity of norovirus genogroup IV: a yearlong monitoring of sewage throughout Italy. Arch Virol. 2010;155:589–93.
- La Rosa G, Fratini M, Spuri Vennarucci V, Guercio A, Purpari G, Muscillo M. GIV noroviruses and other enteric viruses in bivalves: a preliminary study. New Microbiol. 2012;35:27–34 .
- Muscillo M, Fratini M, Graffeo R, Sanguinetti M, Martella V, Green KY, GIV noroviruses in wastewaters and in stool specimens from hospitalized patients. Food Environ Virol. 2013
- Martella V, Campolo M, Lorusso E, Cavicchio P, Camero M, Bellacicco AL, Norovirus in captive lion cub (Panthera leo). Emerg Infect Dis.2007;13:1071–3.
- Martella V, Lorusso E, Decaro N, Elia G, Radogna A, D’Abramo M, Detection and molecular characterization of a canine norovirus. Emerg Infect Dis.2008;14:1306–8.
- Pinto P, Wang Q, Chen N, Dubovi EJ, Daniels JB, Millward LM, Discovery and genomic characterization of noroviruses from a gastroenteritis outbreak in domestic cats in the US. PLoS ONE. 2012;7:e32739.
- Wang QH, Han M, Cheethaam S, Sousa M, Funk JA, Saif LJ. Porcine noroviruses related to human noroviruses. Emerg Infect Dis. 2005;11:1874–81.
- Summa M, von Bonsdorff CH, Maunula L. Pet dogs—a transmission route for human noroviruses? J Clin Virol. 2012;53:244–7.
- Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol.2006;80:10372–81.
- Souza M, Azevedo MS, Jung K, Cheetham S, Saif LJ. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4–HS66 strain of human norovirus. J Virol. 2008;82:1777–86.
- Eden JS, Lim KL, White PA. Complete genome of the human norovirus GIV.1 strain Lake Macquarie virus. J Virol. 2012;86:10251–2.
- Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol. 2009;83:11890–901.
- Di Martino B, Marsilio F, Di Profio F, Lorusso E, Friedrich KG, Buonavoglia C, Detection of antibodies against norovirus genogroup GIV in carnivores.Clin Vaccine Immunol. 2010;17:180–2.
- Bok K, Parra GI, Mitra T, Abente E, Shaver CK, Boon D, Chimpanzees as an animal model for human norovirus infection and vaccine development.Proc Natl Acad Sci U S A. 2011;108:325–30.
- Jiang X, Wilton N, Zhong WM, Farkas T, Huang PW, Barrett E, Diagnosis of human calicivirus by use of enzyme immunoassays. J Infect Dis.2000;181:S349–59 .
- Peasey AE, Ruiz-Palacios GM, Quigley M, Newsholme W, Martinez J, Rosales G, Seroepidemiology and risk factors for sporadic norovirus/Mexico strain. J Infect Dis. 2004;189:2027–36.
- Farkas T, Nakajima S, Sugieda M, Deng X, Zhong WM, Jiang X. Seroprevalence of noroviruses in swine. J Clin Microbiol. 2005;43:657–61.
- Gray JJ, Jiang X, Morgan-Capner P, Desselberger U, Estes MK. Prevalence of antibodies to Norwalk virus in England: detection by enzyme-linked immunosorbent assay using baculovirus-expressed Norwalk virus capsid antigen. J Clin Microbiol. 1993;31:1022–5 .
- Jing Y, Qian Y, Huo Y, Wang LP, Jiang X. Seroprevalence against Norwalk-like human caliciviruses in Beijing, China. J Med Virol. 2000;60:97–101.
- Jiang X, Matson DO, Ruiz-Palacios GM, Hu J, Treanor J, Pickering LK. Expression, self-assembly, and antigenicity of a snow mountain agent-like calicivirus capsid protein. J Clin Microbiol. 1995;33:1452–5 .
- Nurminen K, Blazevic V, Huhti L, Räsänem S, Koho T, Hytönen VP, Prevalence of norovirus GII.4 antibodies in Finnish children. J Med Virol.2011;83:525–31.
- Farkas T, Thornton SA, Wilton N, Zhong W, Altaye M, Jiang X. Homologous versus heterologous immune responses to Norwalk-like viruses among crew members after acute gastroenteritis outbreaks on 2 US Navy vessels. J Infect Dis. 2003;187:187–93.
- Mesquita JR, Costantini VP, Cannon JL, Lin SC, Nascimento MS, Vinjé J. Presence of antibodies against genogroup VI norovirus in humans. Virol J.2013;10:176.
- Pelosi E, Lambden PR, Caul EO, Liu B, Dingle K, Deng Y, The seroepidemiology of genogroup 1 and genogroup 2 Norwalk-like viruses in Italy. J Med Virol. 1999;58:93–9.
- Honma S, Nakata S, Numata K, Kogawa K, Yamashita T, Oseto M, Epidemiological study of prevalence of genogroup II human calicivirus (Mexico virus) infections in Japan and Southeast Asia as determined by enzyme-linked immunosorbent assays. J Clin Microbiol. 1998;36:2481–4 .
- Son H, Jeong HS, Cho M, Lee J, Lee H, Yoon K, Seroepidemiology of predominant norovirus strains circulating in Korea by using recombinant virus-like particle antigens. Foodborne Pathog Dis. 2013;10:461–6.
Suggested citation for this article: Di Martino B, Di Profio F, Ceci C, Di Felice E, Green KY, Bok K, et al. Seroprevalence of norovirus genogroup IV antibodies among humans, Italy, 2010–2011. Emerg Infect Dis. 2014 Nov [date cited]. http://dx.doi.org/10.3201/eid2011.131601