[en] Noroviruses are recognized as the major global cause of sporadic and epidemic non-bacterial gastroenteritis in humans. Molecular mechanisms driving norovirus evolution are the accumulation of point mutations and recombination. Intragenotypic recombination has long been postulated to be a driving force of GII.4 noroviruses, the predominant genotype circulating in humans for over two decades. Increasingly, emergence and re-emergence of different intragenotype recombinants have been reported. The number and types of norovirus recombinants remained undefined until the 2007 JGenVirol research article ‘Norovirus recombination’ reported an assembly of 20 hitherto unclassified intergenotypic norovirus recombinant types. In the intervening decade, a host of novel recombinants has been analysed. New recombination breakpoints have been described, in vitro and in vivo studies supplement in silico analyses, and advances have been made in analysing factors driving norovirus recombination. This work presents a timely overview of these data and focuses on important aspects of norovirus recombination and its role in norovirus molecular evolution. An overview of intergenogroup, intergenotype, intragenotype and ‘obligatory’ norovirus recombinants as detected via in silico methods in the field is provided, enlarging the scope of intergenotypic recombinant types to 80 in total, and notably including three intergenogroup recombinants. A recap of advances made studying norovirus recombination in the laboratory is given. Putative drivers and constraints of norovirus recombination are discussed and the potential link between recombination and norovirus zoonosis risk is examined.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Ludwig, Louisa ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Virologie vétérinaire et maladies virales animales
Mauroy, Axel
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Virologie vétérinaire et maladies virales animales
Language :
English
Title :
Norovirus recombinants: recurrent in the field, recalcitrant in the lab – a scoping review of recombination and recombinant types of noroviruses
Publication date :
2018
Journal title :
Journal of General Virology
ISSN :
0022-1317
eISSN :
1465-2099
Publisher :
Society for General Microbiology, United Kingdom
Volume :
99
Pages :
27-32
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Fonds Léon Fredericq [BE] DADD - Deutscher Akademischer Austauschdienst [DE] Service public fédéral Service Santé Publique, Séecurité de la Chaîne alimentaire et Environnement
Clarke, I.N., Estes, M.K., Green, K.Y., Hansman, G., Knowles, N.J., (2012), Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier
Scipioni, A., Mauroy, A., Vinjé, J., Thiry, E., Animal noroviruses (2008) Vet J, 178, pp. 32-45
Karst, S.M., Zhu, S., Goodfellow, I.G., The molecular pathology of noroviruses (2015) J Pathol, 235, pp. 206-216
Patel, M.M., Widdowson, M.A., Glass, R.I., Akazawa, K., Vinjé, J., Systematic literature review of role of noroviruses in sporadic gastroenteritis (2008) Emerg Infect Dis, 14, pp. 1224-1231
Thorne, L.G., Goodfellow, I.G., Norovirus gene expression and replication (2014) J Gen Virol, 95, pp. 278-291
Taube, S., Kolawole, A.O., Höhne, M., Wilkinson, J.E., Handley, S.A., A mouse model for human norovirus (2013) Mbio, 4, pp. e00450-13
Jones, M.K., Grau, K.R., Costantini, V., Kolawole, A.O., De Graaf, M., Human norovirus culture in B cells (2015) Nat Protoc, 10, pp. 1939-1947
Ettayebi, K., Crawford, S.E., Murakami, K., Broughman, J.R., Karandikar, U., Replication of human noroviruses in stem cell-derived human enteroids (2016) Science, 353, pp. 1387-1393
Wobus, C.E., Thackray, L.B., Virgin, H.W., Murine norovirus: A model system to study norovirus biology and pathogenesis (2006) J Virol, 80, pp. 5104-5112
Wobus, C.E., Karst, S.M., Thackray, L.B., Chang, K.O., Sosnovtsev, S.V., Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages (2004) Plos Biol, 2
McFadden, N., Bailey, D., Carrara, G., Benson, A., Chaudhry, Y., Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4 (2011) Plos Pathog, 7
Vinjé, J., Advances in laboratory methods for detection and typing of norovirus (2015) J Clin Microbiol, 53, pp. 373-381
Kroneman, A., Vega, E., Vennema, H., Vinjé, J., White, P.A., Proposal for a unified norovirus nomenclature and genotyping (2013) Arch Virol, 158, pp. 2059-2068
Andino, R., Domingo, E., Viral quasispecies (2015) Virology, 479-480, pp. 46-51
Posada, D., Crandall, K.A., Holmes, E.C., Recombination in evolutionary genomics (2002) Annu Rev Genet, 36, pp. 75-97
Pérez-Losada, M., Arenas, M., Galán, J.C., Palero, F., González-Candelas, F., Recombination in viruses: Mechanisms, methods of study, and evolutionary consequences (2015) Infect Genet Evol, 30, pp. 296-307
Malim, M.H., Emerman, M., HIV-1 sequence variation: Drift, shift, and attenuation (2001) Cell, 104, pp. 469-472
Jackwood, M.W., Boynton, T.O., Hilt, D.A., McKinley, E.T., Kissinger, J.C., Emergence of a group 3 coronavirus through recombination (2010) Virology, 398, pp. 98-108
Simon-Loriere, E., Holmes, E.C., Why do RNA viruses recombine? (2011) Nat Rev Microbiol, 9, pp. 617-626
Eden, J.S., Tanaka, M.M., Boni, M.F., Rawlinson, W.D., White, P.A., Recombination within the pandemic norovirus GII.4 lineage (2013) J Virol, 87, pp. 6270-6282
Bruggink, L., Catton, M., Marshall, J., A norovirus intervariant GII.4 recombinant in Victoria, Australia, June 2016: The next epidemic variant? (2016) Eurosurveillance, 21, pp. 1-7
Martella, V., Medici, M.C., De Grazia, S., Tummolo, F., Calderaro, A., Evidence for recombination between pandemic GII.4 norovirus strains New Orleans 2009 and Sydney 2012 (2013) J Clin Microbiol, 51, pp. 3855-3857
De Graaf, M., Van Beek, J., Vennema, H., Podkolzin, A.T., Hewitt, J., Emergence of a novel GII.17 norovirus-End of the GII.4 era? (2015) Euro Surveill, 20, p. 21178
Fu, J.G., Shi, C., Xu, C., Lin, Q., Zhang, J., Outbreaks of acute gastroenteritis associated with a re-emerging GII.P16-GII.2 norovirus in the spring of 2017 in Jiangsu, China (2017) Plos One, 12
Bruggink, L.D., Dunbar, N.L., Marshall, J.A., Emergence of GII.E as a major ORF 1 norovirus genotype and its associated ORF 2 GII.4 variant forms (2014) Infect Genet Evol, 22, pp. 157-163
Bruggink, L.D., Dunbar, N.L., Marshall, J.A., Emergence of GII.Pg norovirus in gastroenteritis outbreaks in Victoria, Australia (2016) J Med Virol, 88, pp. 1521-1528
Hoffmann, D., Mauroy, A., Seebach, J., Simon, V., Wantia, N., New norovirus classified as a recombinant GII.G/GII.1 causes an extended foodborne outbreak at a university hospital in Munich (2013) J Clin Virol, 58, pp. 24-30
Van Beek, J., De Graaf, M., Al-Hello, H., Allen, D.J., Ambert-Balay, K., Molecular surveillance of norovirus, 2005-16: An epidemiological analysis of data collected from the NoroNet network (2018) Lancet Infect Dis, p. 18. , Epub ahead of print
Mahar, J.E., Bok, K., Green, K.Y., Kirkwood, C.D., The importance of intergenic recombination in norovirus GII.3 evolution (2013) J Virol, 87, pp. 3687-3698
Thackray, L.B., Wobus, C.E., Chachu, K.A., Liu, B., Alegre, E.R., Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence (2007) J Virol, 81, pp. 10460-10473
Bull, R.A., Tanaka, M.M., White, P.A., Norovirus recombination (2007) J Gen Virol, 88, pp. 3347-3359
Kroneman, A., Vennema, H., Deforche, K., Avoort, H., Peñaranda, S., An automated genotyping tool for enteroviruses and noroviruses (2011) J Clin Virol, 51, pp. 121-125
Waters, A., Coughlan, S., Hall, W.W., Characterisation of a novel recombination event in the norovirus polymerase gene (2007) Virology, 363, pp. 11-14
Siqueira, J., Bandeira, R., Justino, M., Linhares, A., Gabbay, Y.B., Characterization of novel intragenotype recombination events among norovirus pandemic GII.4 variants (2016) Infect Genet Evol, 44, pp. 361-366
Cai, H., Yu, Y., Jin, M., Pan, Y., Yan, S., Cloning, sequencing and characterization of the genome of a recombinant norovirus of the rare genotype GII.P7/GII.6 in China (2017) Arch Virol, 162, pp. 2053-2059
Chhabra, P., Walimbe, A.M., Chitambar, S.D., Complete genome characterization of Genogroup II norovirus strains from India: Evidence of recombination in ORF2/3 overlap (2010) Infect Genet Evol, 10, pp. 1101-1109
Kamel, A.H., Ali, M.A., El-Nady, H.G., De Rougemont, A., Pothier, P., Predominance and circulation of enteric viruses in the region of greater Cairo, Egypt (2009) J Clin Microbiol, 47, pp. 1037-1045
Motomura, K., Yokoyama, M., Ode, H., Nakamura, H., Mori, H., Divergent evolution of norovirus GII/4 by genome recombination from May 2006 to February 2009 in Japan (2010) J Virol, 84, pp. 8085-8097
Lam, T.T., Zhu, H., Smith, D.K., Guan, Y., Holmes, E.C., The recombinant origin of emerging human norovirus GII.4/2008: Intragenotypic exchange of the capsid P2 domain (2012) J Gen Virol, 93, pp. 817-822
Supadej, K., Khamrin, P., Kumthip, K., Kochjan, P., Yodmeeklin, A., Wide variety of recombinant strains of norovirus GII in pediatric patients hospitalized with acute gastroenteritis in Thailand during 2005 to 2015 (2017) Infect Genet Evol, 52, pp. 44-51
Zhang, H., Cockrell, S.K., Kolawole, A.O., Rotem, A., Serohijos, A., Isolation and analysis of rare norovirus recombinants from Coinfected Mice Using Drop-Based Microfluidics (2015) J Virol, 89, pp. 7722-7734
Lowry, K., Woodman, A., Cook, J., Evans, D.J., Recombination in enteroviruses is a biphasic replicative process involving the generation of greater-than genome length ’imprecise’ intermediates (2014) Plos Pathog, 10
Gallei, A., Pankraz, A., Thiel, H.J., Becher, P., RNA recombination in vivo in the absence of viral replication (2004) J Virol, 78, pp. 6271-6281
Kleine Büning, M., Meyer, D., Austermann-Busch, S., Roman-Sosa, G., Rümenapf, T., Nonreplicative RNA recombination of an animal plus-strand RNA virus in the absence of efficient translation of viral proteins (2017) Genome Biol Evol, 9, pp. 817-829
Galli, A., Bukh, J., Comparative analysis of the molecular mechanisms of recombination in hepatitis C virus (2014) Trends Microbiol, 22, pp. 354-364
Bagaya, B.S., Tian, M., Nickel, G.C., Vega, J.F., Li, Y., An in vitro model to mimic selection of replication-competent HIV-1 intersubtype recombination in dual or superinfected patients (2017) J Mol Biol, 429, pp. 2246-2264
Hardy, M.E., Kramer, S.F., Treanor, J.J., Estes, M.K., Human calicivirus genogroup II capsid sequence diversity revealed by analyses of the prototype Snow Mountain agent (1997) Arch Virol, 142, pp. 1469-1479
Etherington, G.J., Dicks, J., Roberts, I.N., High throughput sequence analysis reveals hitherto unreported recombination in the genus Norovirus (2006) Virology, 345, pp. 88-95
Lauring, A.S., Ino, R., Quasispecies theory and the behavior of RNA viruses (2010) Plos Pathog, p. 6. , e1001005-e1001008
Cannon, J.L., Barclay, L., Collins, N.R., Wikswo, M.E., Castro, C.J., Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses (2017) J Clin Microbiol, 55, pp. 2208-2221
Botha, J.C., Taylor, M.B., Mans, J., Comparative analysis of South African norovirus GII.4 strains identifies minor recombinant variants (2017) Infect Genet Evol, 47, pp. 26-34
Giammanco, G.M., Rotolo, V., Medici, M.C., Tummolo, F., Bonura, F., Recombinant norovirus GII.G/GII.12 gastroenteritis in children (2012) Infect Genet Evol, 12, pp. 169-174
Bruggink, L.D., Moselen, J.M., Marshall, J.A., Genotype analysis of noroviruses associated with gastroenteritis outbreaks in childcare centres, Victoria, Australia, 2012-2015 (2017) Epidemiol Infect, 145, pp. 1933-1941
Arana, A., Cilla, G., Montes, M., Gomariz, M., Pérez-Trallero, E., Genotypes, recombinant forms, and variants of norovirus GII.4 in Gipuzkoa (Basque Country, Spain), 2009-2012 (2014) Plos One, 9
Mans, J., Murray, T.Y., Taylor, M.B., Novel norovirus recombinants detected in South Africa (2014) Virol J, 11, pp. 168-169
Lim, K.L., Hewitt, J., Sitabkhan, A., Eden, J.S., Lun, J., A multi-site study of norovirus molecular epidemiology in Australia and New Zealand, 2013-2014 (2016) Plos One, 11
Hasing, M.E., Hazes, B., Lee, B.E., Preiksaitis, J.K., Pang, X.L., Detection and analysis of recombination in GII.4 norovirus strains causing gastroenteritis outbreaks in Alberta (2014) Infect Genet Evol, 27, pp. 181-192
Bruggink, L.D., Marshall, J.A., Molecular and epidemiological features of GIIb norovirus outbreaks in Victoria, Australia, 2002-2005 (2009) J Med, 81, pp. 1652-1660
Bruggink, L.D., Marshall, J.A., Altered patterns of norovirus GII.B recombinant forms in gastroenteritis outbreaks in Victoria, Australia, 2002-2005 compared to 2006-2011 (2013) J Med Virol, 85, pp. 1433-1443
Eden, J.S., Bull, R.A., Tu, E., McIver, C.J., Lyon, M.J., Norovirus GII.4 variant 2006b caused epidemics of acute gastroenteritis in Australia during 2007 and 2008 (2010) J Clin Virol, 49, pp. 265-271
Mathijs, E., Denayer, S., Palmeira, L., Botteldoorn, N., Scipioni, A., Novel norovirus recombinants and of GII.4 sub-lineages associated with outbreaks between 2006 and 2010 in Belgium (2011) Virol J, 8, p. 310
Symes, S.J., Gunesekere, I.C., Marshall, J.A., Wright, P.J., Norovirus mixed infection in an oyster-associated outbreak: An opportunity for recombination (2007) Arch Virol, 152, pp. 1075-1086
Johnson, J.A., Parra, G.I., Levenson, E.A., Green, K.Y., A large outbreak of acute gastroenteritis in Shippensburg, Pennsylvania, 1972 revisited: Evidence for common source exposure to a recombinant GII.Pg/GII.3 norovirus (2017) Epidemiol Infect, 145, pp. 1591-1596
Woodman, A., Arnold, J.J., Cameron, C.E., Evans, D.J., Biochemical and genetic analysis of the role of the viral polymerase in enterovirus recombination (2016) Nucleic Acids Res, 44, pp. 6883-6895
Mathijs, E., Muylkens, B., Mauroy, A., Ziant, D., Delwiche, T., Experimental evidence of recombination in murine noroviruses (2010) J Gen Virol, 91, pp. 2723-2733
Mathijs, E., Oliveira-Filho, E.F., Dal Pozzo, F., Mauroy, A., Thiry, D., Infectivity of a recombinant murine norovirus (RecMNV) in Balb/cByJ mice (2016) Vet Microbiol, 192, pp. 118-122
Tao, Y., Rotem, A., Zhang, H., Cockrell, S.K., Koehler, S.A., Artifact-Free quantification and sequencing of rare recombinant viruses by using drop-based microfluidics (2015) Chembiochem, 16, pp. 2167-2171
Muylkens, B., Farnir, F., Meurens, F., Schynts, F., Vanderplasschen, A., Coinfection with two closely related alphaherpesviruses results in a highly diversified recombination mosaic displaying negative genetic interference (2009) J Virol, 83, pp. 3127-3137
Symes, S.J., Job, N., Ficorilli, N., Hartley, C.A., Browning, G.F., Novel assay to quantify recombination in a calicivirus (2015) Vet Microbiol, 177, pp. 25-31
Müller, B., Klemm, U., Mas Marques, A., Schreier, E., Genetic diversity and recombination of murine noroviruses in immunocompromised mice (2007) Arch Virol, 152, pp. 1709-1719
Worobey, M., Holmes, E.C., Evolutionary aspects of recombination in RNA viruses (1999) J Gen Virol, 80, pp. 2535-2543
Utsumi, T., Lusida, M.I., Dinana, Z., Wahyuni, R.M., Yamani, L.N., Occurrence of norovirus infection in an asymptomatic population in Indonesia (2017) Infect Genet Evol, 55, pp. 1-7
Pringle, K., Lopman, B., Vega, E., Vinje, J., Parashar, U.D., Noroviruses: Epidemiology, immunity and prospects for prevention (2015) Future Microbiol, 10, pp. 53-67
Lopman, B., Simmons, K., Gambhir, M., Vinjé, J., Parashar, U., Epidemiologic implications of asymptomatic reinfection: A mathematical modeling study of norovirus (2014) Am J Epidemiol, 179, pp. 507-512
Vega, E., Donaldson, E., Huynh, J., Barclay, L., Lopman, B., RNA populations in immunocompromised patients as reservoirs for novel norovirus variants (2014) J Virol, 88, pp. 14184-14196
Karst, S.M., Baric, R.S., What is the reservoir of emergent human norovirus strains? (2015) J Virol, 89, pp. 5756-5759
De Graaf, M., Van Beek, J., Koopmans, M.P., Human norovirus transmission and evolution in a changing world (2016) Nat Rev Microbiol, 14, pp. 421-433
Lysén, M., Thorhagen, M., Brytting, M., Hjertqvist, M., Ersson, Y., Genetic diversity among food-borne and waterborne norovirus strains causing outbreaks in Sweden (2009) J Clin Microbiol, 47, pp. 2411-2418
Karst, S.M., Wobus, C.E., A working model of how noroviruses infect the intestine (2015) Plos Pathog, 11
Atmar, R.L., Opekun, A.R., Gilger, M.A., Estes, M.K., Crawford, S.E., Determination of the 50% human infectious dose for Norwalk virus (2014) J Infect Dis, 209, pp. 1016-1022
Sackman, A.M., Reed, D., Rokyta, D.R., Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages (2015) Peerj, 3
White, P.A., Evolution of norovirus (2014) Clin Microbiol Infect, 20, pp. 741-745
Boon, D., Mahar, J.E., Abente, E.J., Kirkwood, C.D., Purcell, R.H., Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period (2011) J Virol, 85, pp. 8656-8666
Mauroy, A., Scipioni, A., Mathijs, E., Ziant, D., Daube, G., Genetic and evolutionary perspectives on genogroup III, genotype 2 bovine noroviruses (2014) Arch Virol, 159, pp. 39-49
Hoffmann, D., Hutzenthaler, M., Seebach, J., Panning, M., Umgelter, A., Norovirus GII.4 and GII.7 capsid sequences undergo positive selection in chronically infected patients (2012) Infect Genet Evol, 12, pp. 461-466
Bank-Wolf, B.R., König, M., Thiel, H.J., Zoonotic aspects of infections with noroviruses and sapoviruses (2010) Vet Microbiol, 140, pp. 204-212
Mathijs, E., Stals, A., Baert, L., Botteldoorn, N., Denayer, S., A review of known and hypothetical transmission routes for noroviruses (2012) Food Environ Virol, 4, pp. 131-152
Wilhelm, B., Waddell, L., Greig, J., Rajić, A., Houde, A., A scoping review of the evidence for public health risks of three emerging potentially zoonotic viruses: Hepatitis E virus, norovirus, and rotavirus (2015) Prev Vet Med, 119, pp. 61-79
Orchard, R.C., Wilen, C.B., Doench, J.G., Baldridge, M.T., McCune, B.T., Discovery of a proteinaceous cellular receptor for a norovirus (2016) Science, 353, pp. 933-936
Takano, T., Kusuhara, H., Kuroishi, A., Takashina, M., Doki, T., Molecular characterization and pathogenicity of a genogroup GVI feline norovirus (2015) Vet Microbiol, 178, pp. 201-207
Yu, Y., Yan, S., Li, B., Pan, Y., Wang, Y., Genetic Diversity and Distribution of Human Norovirus in China (1999-2011) (2014) Biomed Res Int 2014, , Epub ahead of print
Katayama, K., Shirato-Horikoshi, H., Kojima, S., Kageyama, T., Oka, T., Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses (2002) Virology, 299, pp. 225-239
Fukuda, S., Sasaki, Y., Takao, S., Seno, M., Recombinant norovirus implicated in gastroenteritis outbreaks in Hiroshima Prefecture, Japan (2008) J Med Virol, 80, pp. 921-928
Jin, M., Chen, J., Zhang, X.H., Zhang, M., Li, H.Y., Genetic diversity of noroviruses in Chinese adults: Potential recombination hotspots and GII-4/Den Haag-specific mutations at a putative epitope (2011) Infect Genet Evol, 11, pp. 1716-1726
Ji, L., Wu, X., Yao, W., Chen, L., Xu, D., Rapid emergence of novel GII.4 sub-lineages noroviruses associated with outbreaks in Huzhou, China, 2008-2012 (2013) Plos One, 8
Nakamura, K., Iwai, M., Zhang, J., Obara, M., Horimoto, E., Detection of a novel recombinant norovirus from sewage water in Toyama Prefecture, Japan (2009) Jpn J Infect Dis, 62, pp. 394-398
Phan, T.G., Kaneshi, K., Ueda, Y., Nakaya, S., Nishimura, S., Genetic heterogeneity, evolution, and recombination in noroviruses (2007) J Med Virol, 79, pp. 1388-1400
Jiang, X., Espul, C., Zhong, W.M., Cuello, H., Matson, D.O., Characterization of a novel human calicivirus that may be a naturally occurring recombinant (1999) Arch Virol, 144, pp. 2377-2387
Gallimore, C.I., Lewis, D., Taylor, C., Cant, A., Gennery, A., Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH) (2004) J Clin Virol, 30, pp. 196-204
Iritani, N., Seto, Y., Kubo, H., Murakami, T., Haruki, K., Prevalence of Norwalk-like virus infections in cases of viral gastroenteritis among children in Osaka City, Japan (2003) J Clin Microbiol, 41, pp. 1756-1759
Martínez, N., Espul, C., Cuello, H., Zhong, W., Jiang, X., Sequence diversity of human caliciviruses recovered from children with diarrhea in Mendoza, Argentina, 1995-1998 (2002) J Med Virol, 67, pp. 289-298
Tsugawa, T., Numata-Kinoshita, K., Honma, S., Nakata, S., Tatsumi, M., Virological, serological, and clinical features of an outbreak of acute gastroenteritis due to recombinant genogroup II norovirus in an infant home (2006) J Clin Microbiol, 44, pp. 177-182
Ambert-Balay, K., Bon, F., Le Guyader, F., Pothier, P., Kohli, E., Characterization of new recombinant noroviruses (2005) J Clin Microbiol, 43, pp. 5179-5186
Bon, F., Ambert-Balay, K., Giraudon, H., Kaplon, J., Le Guyader, S., Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004 (2005) J Clin Microbiol, 43, pp. 4659-4664
Phan, T.G., Takanashi, S., Kaneshi, K., Ueda, Y., Nakaya, S., Detection and genetic characterization of norovirus strains circulating among infants and children with acute gastroenteritis in Japan during 2004-2005 (2006) Clin Lab, 52, pp. 519-525
Reuter, G., Vennema, H., Koopmans, M., Szücs, G., Epidemic spread of recombinant noroviruses with four capsid types in Hungary (2006) J Clin Virol, 35, pp. 84-88
Vidal, R., Roessler, P., Solari, V., Vollaire, J., Jiang, X., Novel recombinant norovirus causing outbreaks of gastroenteritis in Santiago, Chile (2006) J Clin Microbiol, 44, pp. 2271-2275
Buesa, J., Collado, B., López-Andújar, P., Abu-Mallouh, R., Diaz, J.R., Molecular epidemiology of caliciviruses causing outbreaks and sporadic cases of acute gastroenteritis in spain molecular epidemiology of caliciviruses causing outbreaks and sporadic cases of acute gastroenteritis in Spain (2002) J Clin Microbiol, 40, pp. 2854-2859
Gallimore, C.I., Cubitt, D., Plessis, N., Jim, J., Gray, J.J., Asymptomatic and Symptomatic excretion of noroviruses during a hospital outbreak of gastroenteritis asymptomatic and symptomatic excretion of noroviruses during a hospital outbreak of gastroenteritis (2004) Society, 42, pp. 9-13
Phan, T.G., Yagyu, F., Kozlov, V., Kozlov, A., Okitsu, S., Viral gastroenteritis and genetic characterization of recombinant norovirus circulating in Eastern Russia (2006) Clin Lab, 52, pp. 247-253
Gallimore, C.I., Cheesbrough, J.S., Lamden, K., Bingham, C., Gray, J.J., Multiple norovirus genotypes characterised from an oysterassociated outbreak of gastroenteritis (2005) Int J Food Microbiol, 103, pp. 323-330
Mahar, J.E., Kirkwood, C.D., Characterization of norovirus strains in Australian children from 2006 to 2008: Prevalence of recombinant strains (2011) J Med Virol, 83, pp. 2213-2219
Wang, Y.H., Zhou, D.J., Zhou, X., Yang, T., Ghosh, S., Molecular epidemiology of noroviruses in children and adults with acute gastroenteritis in Wuhan, China, 2007-2010 (2012) Arch Virol, 157, pp. 2417-2424
Truong, T.C., Than, V.T., Kim, W., Evolutionary phylodynamics of Korean noroviruses reveals a novel GII.2/GII.10 recombination event (2014) Plos One, 9
Lu, Q.B., Huang, D.D., Zhao, J., Wang, H.Y., Zhang, X.A., An increasing prevalence of recombinant GII norovirus in pediatric patients with diarrhea during 2010-2013 in China (2015) Infect Genet Evol, 31, pp. 48-52
Phumpholsup, T., Chieochansin, T., Vongpunsawad, S., Vuthitanachot, V., Payungporn, S., Human norovirus genogroup II recombinants in Thailand, 2009-2014 (2015) Arch Virol, 160, pp. 2603-2609
Fu, J.G., Ai, J., Zhang, J., Wu, Q.B., Qi, X., Molecular epidemiology of genogroup II norovirus infection among hospitalized children with acute gastroenteritis in Suzhou (Jiangsu, China) from 2010 to 2013 (2016) J Med Virol, p. 88
Ping, J.L., Qian, Y., Zhang, Y., Deng, L., Ying, L.L., Prevalence and genetic diversity of noroviruses in outpatient pediatric clinics in Beijing, China 2010-2012 (2014) Infect Genet Evol, 28, pp. 71-77
Fumian, T.M., Da Silva Ribeiro De Andrade, J., Leite, J.P., Miagostovich, M.P., Norovirus recombinant strains isolated from gastroenteritis outbreaks in Southern Brazil, 2004-2011 (2016) Plos One, 11
Chhabra, P., Dhongade, R.K., Kalrao, V.R., Bavdekar, A.R., Chitambar, S.D., Epidemiological, clinical, and molecular features of norovirus infections in western India (2009) J Med Virol, 81, pp. 922-932
Nayak, M.K., Chatterjee, D., Nataraju, S.M., Pativada, M., Mitra, U., A new variant of Norovirus GII.4/2007 and inter-genotype recombinant strains of NVGII causing acute watery diarrhoea among children in Kolkata, India (2009) J Clin Virol, 45, pp. 223-229
Han, T.H., Kim, C.H., Chung, J.Y., Park, S.H., Hwang, E.S., Emergence of norovirus GII-4/2008 variant and recombinant strains in Seoul, Korea (2011) Arch Virol, 156, pp. 323-329
Chung, J.Y., Han, T.H., Park, S.H., Kim, S.W., Hwang, E.S., Detection of GII-4/2006b variant and recombinant noroviruses in children with acute gastroenteritis, South Korea (2010) J Med Virol, 82, pp. 146-152
Chhabra, P., Walimbe, A.M., Chitambar, S.D., Molecular characterization of three novel intergenotype norovirus GII recombinant strains from western India (2010) Virus Res, 147, pp. 242-246
Dai, Y.C., Hu, G.F., Zhang, X.F., Song, C.L., Xiang, W.L., Molecular epidemiology of norovirus gastroenteritis in children in Jiangmen, China, 2005-2007 (2011) Arch Virol, 156, pp. 1641-1646
Jia, L.P., Qian, Y., Zhang, Y., Deng, L., Liu, L.Y., Prevalence and genetic diversity of noroviruses in outpatient pediatric clinics in Beijing, China 2010-2012 (2014) Infect Genet Evol, 28, pp. 71-77
Hernandez, J., Silva, L., Sousa, E.C., Lucena, M., Soares, L., Analysis of uncommon norovirus recombinants from Manaus, Amazon region, Brazil: GII.P22/GII.5, GII.P7/GII.6 and GII.Pg/GII.1 (2016) Infect Genet Evol, 39, pp. 365-371
Thongprachum, A., Okitsu, S., Khamrin, P., Maneekarn, N., Hayakawa, S., Emergence of norovirus GII.2 and its novel recombination during the gastroenteritis outbreak in Japanese children in mid-2016 (2017) Infect Genet Evol, 51, pp. 86-88
Barreira, D., Fumian, T.M., Tonini, M., Volpini, L., Santos, R.P., Detection and molecular characterization of the novel recombinant norovirus GII.P16-GII.4 Sydney in southeastern Brazil in 2016 (2017) Plos One, 12, pp. 1-9
Puustinen, L., Blazevic, V., Salminen, M., Hämäläinen, M., Räsänen, S., Noroviruses as a major cause of acute gastroenteritis in children in Finland, 2009-2010 (2011) Scand J Infect Dis, 43, pp. 804-808
Takanashi, S., Wang, Q., Chen, N., Shen, Q., Jung, K., Characterization of emerging GII.G/GII.12 noroviruses from a gastroenteritis outbreak in the United States in 2010 (2011) J Clin Microbiol, 49, pp. 3234-3244
Lodo, K.L., Veitch, M.G., Green, M.L., An outbreak of norovirus linked to oysters in Tasmania (2014) Commun Dis Intell Q Rep, 38, pp. E16-E19
Loury, P., Le Guyader, F.S., Le Saux, J.C., Ambert-Balay, K., Parrot, P., A norovirus oyster-related outbreak in a nursing home in France, January 2012 (2015) Epidemiol Infect, 143, pp. 2486-2493
Medici, M.C., Tummolo, F., Martella, V., Chezzi, C., Arcangeletti, M.C., Epidemiological and molecular features of norovirus infections in Italian children affected with acute gastroenteritis (2014) Epidemiol Infect, 142, pp. 2326-2335
Vega, E., Vinjé, J., Novel GII.12 norovirus strain, United States, 2009-2010 (2011) Emerg Infect Dis, 17, pp. 1516-1518
Sang, S., Zhao, Z., Suo, J., Xing, Y., Jia, N., Report of recombinant Norovirus GII.G/GII.12 in Beijing, China (2014) Plos One, 9
Zeng, M., Gong, Z., Zhang, Y., Zhu, Q., Wang, X., Prevalence and genetic diversity of norovirus in outpatient children with acute diarrhea in Shanghai, China (2011) Jpn J Infect Dis, 64, pp. 417-422
Dey, S.K., Phan, T.G., Mizuguchia, M., Okitsua, S., Ushijima, H., Novel recombinant norovirus in Japan (2010) Virus Genes, 40, pp. 362-364
Jin, M., Xie, H.P., Duan, Z.J., Liu, N., Zhang, Q., Emergence of the GII4/2006b variant and recombinant noroviruses in China (2008) J Med Virol, 80, pp. 1997-2004
Sai, L., Wang, G., Shao, L., Liu, H., Zhang, Y., Clinical and molecular epidemiology of norovirus infection in adults with acute gastroenteritis in Ji’nan, China (2013) Arch Virol, 158, pp. 2315-2322
Shen, Q., Zhang, W., Yang, S., Chen, Y., Shan, T., Genomic organization and recombination analysis of human norovirus identified from China (2012) Mol Biol Rep, 39, pp. 1275-1281
Hansman, G.S., Katayama, K., Maneekarn, N., Peerakome, S., Khamrin, P., Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand (2004) J Clin Microbiol, 42, pp. 1305-1307
Rackoff, L.A., Bok, K., Green, K.Y., Kapikian, A.Z., Epidemiology and evolution of rotaviruses and noroviruses from an archival WHO Global Study in Children (1976-79) with implications for vaccine design (2013) Plos One, 8
Nahar, S., Afrad, M.H., Fahmi, T., Moni, S., Haque, W., A novel norovirus recombinant strain GII.4/GII.21 in Bangladesh, 2011 (2013) Virus Genes, 46, pp. 538-541
Phan, T.G., Yan, H., Li, Y., Okitsu, S., Müller, W.E., Novel recombinant norovirus in China (2006) Emerg Infect Dis, 12, pp. 857-858
Sasaki, Y., Kai, A., Hayashi, Y., Noguchi, Y., Hasegawa, M., (2006) Multiple Viral Infections and Genomic Divergence among Noroviruses during an Outbreak of Acute Gastroenteritis Multiple Viral Infections and Genomic Divergence among Noroviruses during an Outbreak of Acute Gastroenteritis, 44, pp. 790-797
Fajardo, Á., Tort, F.L., Victoria, M., Fumian, T.M., Miagostovich, M.P., Phylogenetic analyses of Norovirus strains detected in Uruguay reveal the circulation of the novel GII.P7/GII.6 recombinant variant (2014) Infect Genet Evol, 28, pp. 328-332
Yang, Z., Vinjé, J., Elkins, C.A., Kulka, M., Complete genome sequence of human norovirus strain GII.P7-GII.6 detected in a patient in the United States in 2014 (2016) Genome Announc, 4, pp. e01211-16
Fumian, T.M., Aragão, G.C., Mascarenhas, J.D., Kaiano, J.H., Siqueira, J.A., Detection of a novel recombinant strain of norovirus in an African-descendant community from the Amazon region of Brazil in 2008 (2012) Arch Virol, 157, pp. 2389-2392
Ruether, I.G., Dimitriou, T.G., Tsakogiannis, D., Kyriakopoulou, Z., Amoutzias, G.D., Characterization of novel intergenogroup and intergenotype recombinant noroviruses from central Greece (2014) Mol Cell Probes, 28, pp. 204-210
Ruether, I.G., Tsakogiannis, D., Pliaka, V., Kyriakopoulou, Z., Krikelis, A., Molecular characterization of a new intergenotype norovirus GII recombinant (2012) Virus Genes, 44, pp. 237-243
Ruether, I.G., Tsakogiannis, D., Kyriakopoulou, Z., Dimitriou, T.G., Papamichail, C., Circulation of intergenotype recombinant noroviruses GII.9/GII.6 from 2006 to 2011 in central Greece (2014) Virus Genes, 48, pp. 23-31
Shen, Q., Zhang, W., Yang, S., Yang, Z., Chen, Y., Recombinant porcine norovirus identified from piglet with diarrhea (2012) BMC Vet Res, 8, p. 155
Won, Y.-J., Park, J.-W., Han, S.-H., Cho, H.-G., Kang, L.-H., Fullgenomic analysis of a human norovirus recombinant GII.12/13 novel strain isolated from South Korea (2013) Plos One, 8
Ayukekbong, J., Lindh, M., Nenonen, N., Tah, F., Nkuo-Akenji, T., Enteric viruses in healthy children in Cameroon: Viral load and genotyping of norovirus strains (2011) J Med Virol, 83, pp. 2135-2142
Kwok, K., Niendorf, S., Lee, N., Hung, T.N., Chan, L.Y., Increased detection of emergent recombinant norovirus GII.P16-GII.2 strains in young adults, Hong Kong, China, 2016-2017 (2017) Emerg Infect Dis, 23, pp. 1852-1855
Niendorf, S., Jacobsen, S., Faber, M., Eis-Hübinger, A.M., Hofmann, J., Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016 (2017) Eurosurveillance, 22, pp. 2-5
Nahar, S., Afrad, M.H., Matthijnssens, J., Rahman, M.Z., Momtaz, Z., Novel intergenotype human norovirus recombinant GII.16/ GII.3 in Bangladesh (2013) Infect Genet Evol, 20, pp. 325-329
Medici, M.C., Tummolo, F., Martella, V., Giammanco, G.M., De Grazia, S., Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy (2014) Virus Res, 188, pp. 142-145
Matsushima, Y., Shimizu, T., Ishikawa, M., Komane, A., Okabe, N., Complete genome sequence of a recombinant GII.P16-GII.4 norovirus detected in Kawasaki City, Japan, in 2016 (2016) Genome Announc, 4, pp. e01099-16
Bidalot, M., Théry, L., Kaplon, J., De Rougemont, A., Ambert-Balay, K., Emergence of new recombinant noroviruses GII.P16-GII.4 and GII.p16-GII.2, France, winter 2016 to 2017 (2017) Euro Surveill, 22, pp. 1-5
Mäde, D., Trübner, K., Neubert, E., Höhne, M., Johne, R., Detection and typing of norovirus from frozen strawberries involved in a large-scale gastroenteritis outbreak in Germany (2013) Food Environ Virol, 5, pp. 162-168
Matsushima, Y., Ishikawa, M., Shimizu, T., Genetic analyses of GII. 17 norovirus strains in diarrheal disease outbreaks from December 2014 to March 2015 in Japan reveal a novel polymerase sequence (2015) Euro, pp. 1-6
Han, M.G., Smiley, J.R., Thomas, C., Saif, L.J., Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses (2004) J Clin Microbiol, 42, pp. 5214-5224
Oliver, S.L., Brown, D.W., Green, J., Bridger, J.C., A chimeric bovine enteric calicivirus: Evidence for genomic recombination in genogroup III of the Norovirus genus of the Caliciviridae (2004) Virology, 326, pp. 231-239
Ferragut, F., Vega, C.G., Mauroy, A., Conceição-Neto, N., Zeller, M., Molecular detection of bovine noroviruses in Argentinean dairy calves: Circulation of a tentative new genotype (2016) Infect Genet Evol, 40, pp. 144-150
Di Felice, E., Mauroy, A., Pozzo, F.D., Thiry, D., Ceci, C., Bovine noroviruses: A missing component of calf diarrhoea diagnosis (2016) Vet J, 207, pp. 53-62
Nayak, M.K., Balasubramanian, G., Sahoo, G.C., Bhattacharya, R., Vinje, J., Detection of a novel intergenogroup recombinant Norovirus from Kolkata, India (2008) Virology, 377, pp. 117-123
Ferreira, M.S., Cubel Garcia, R.C., Xavier, M.P., Ribeiro, R.L., Assis, R.M., Genotyping of gastroenteric viruses in hospitalised children: First report of norovirus GII.21 in Brazil (2012) Mem Inst Oswaldo Cruz, 107, pp. 1064-1067