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The Dynamics of Norovirus Outbreak Epidemics: Recent Insights

DOI: 10.3390/ijerph8041141

Keywords: norovirus, outbreaks, epidemics, genetic factors, environmental factors

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Noroviruses are a major cause of gastroenteritis outbreaks worldwide. Norovirus outbreaks frequently occur as epidemics which appear to be related to both genetic and environmental factors. This review considers recent progress in understanding these factors. The norovirus genome undergoes continuous change and this appears to be important in the persistence of the virus in the community. Studies on the common GII.4 genotype have shown that some norovirus outbreak epidemics involving this genotype are correlated with specific changes in the genome. In contrast to the growing understanding of the role of genetic factors in norovirus outbreak epidemics, the role of environmental factors is less well understood. Topics reviewed here include long term excretion of norovirus in some individuals, long term survivability of norovirus in the environment, the role of meteorological factors in the control of norovirus outbreaks and the possible zoonotic transmission of the virus.


[1]  Marshall, JA; Bruggink, LD. Laboratory diagnosis of norovirus. Clin. Lab 2006, 52, 571–581.
[2]  Friedman, GD. Primer of Epidemiology, 5th ed ed.; McGraw-Hill: New York, NY, USA, 2004; p. 79.
[3]  Bruggink, LD; Marshall, JA. Molecular changes associated with altered patterns of norovirus outbreak epidemics in Victoria, Australia, in 2006 to 2007. J. Clin. Microbiol 2010, 48, 857–861.
[4]  Bruggink, LD; Marshall, JA. Norovirus epidemics are linked to two distinct sets of controlling factors. Int. J. Infect. Dis 2009, 13, e125–e126.
[5]  Siebenga, JJ; Vennema, H; Zheng, DP; Vinje, J; Lee, BE; Pang, XL; Ho, ECM; Lim, W; Choudekar, A; Broor, S; et al. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J. Infect. Dis 2009, 200, 802–812.
[6]  Thackray, LB; Wobus, CE; Chachu, KA; Liu, B; Alegre, ER; Henderson, KS; Kelley, ST; Virgin, HW. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J. Virol 2007, 81, 10460–10473.
[7]  Zheng, DP; Ando, T; Fankhauser, RL; Beard, RS; Glass, RI; Monroe, SS. Norovirus classification and proposed strain nomenclature. Virology 2006, 346, 312–323.
[8]  Patel, MM; Hall, AJ; Vinje, J; Parashar, UD. Noroviruses: A comprehensive review. J. Clin. Virol 2009, 44, 1–8.
[9]  Vinje, J; Hamidjaja, RA; Sobsey, MD. Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J. Virol. Methods 2004, 116, 109–117.
[10]  Green, KY. Caliciviridae: The noroviruses. In Fields Virology, 5th ed; Knipe, DM, Howley, PM, Eds.; Wolters Kluwer/Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; Volume 1. Chapter 28,, pp. 949–979.
[11]  Burton-MacLeod, JA; Kane, EM; Beard, RS; Hadley, LA; Glass, RI; Ando, T. Evaluation and comparison of two commercial enzyme-linked immunosorbent assay kits for detection of antigenically diverse human noroviruses in stool samples. J. Clin. Microbiol 2004, 42, 2587–2595.
[12]  Scipioni, A; Mauroy, A; Vinje, J; Thiry, E. Animal noroviruses. Vet. J 2008, 178, 32–45.
[13]  Tan, M; Jiang, X. Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathogens 2010, 6, e1000983.
[14]  Donaldson, EF; Lindesmith, LC; Lobue, AD; Baric, RS. Norovirus pathogenesis: Mechanisms of persistence and immune evasion in human populations. Immunol. Rev 2008, 225, 190–211.
[15]  Bok, K; Abente, EJ; Realpe-Quintero, M; Mitra, T; Sosnovtsev, SV; Kapikian, AZ; Green, KY. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J. Virol 2009, 83, 11890–11901.
[16]  Siebenga, JJ; Lemey, P; Kosakovsky Pond, SL; Rambout, A; Vennema, H; Koopmans, M. Phylodynamic reconstruction reveals norovirus GII.4 epidemic expansions and their molecular determinants. PLoS Pathogens 2010, 6, e1000884.
[17]  Dingle, KE; Norovirus Infection Control in Oxfordshire Communities Hospitals. Mutation in a Lordsdale norovirus epidemic strain as a potential indicator of transmission routes. J. Clin. Microbiol 2004, 42, 3950–3957.
[18]  Bull, RA; Tanaka, MM; White, PA. Norovirus recombination. J. Gen. Virol 2007, 88, 3347–3359.
[19]  Rohayem, J; Munch, J; Rethwilm, A. Evidence of recombination in the norovirus capsid gene. J. Virol 2005, 79, 4977–4990.
[20]  Motomura, K; Yokoyama, M; Ode, H; Nakamura, H; Mori, H; Kanda, T; Oka, T; Katayama, K; Noda, M; Tanaka, T; Takeda, N; Sato, H; the Norovirus Surveillance Group of Japan. Divergent evolution of norovirus GII/4 by genome recombination from May 2006 to February 2009 in Japan. J. Virol 2010, 84, 8085–8097.
[21]  Bailey, D; Thackray, LB; Goodfellow, IG. A single amino acid substitution in the murine norovirus capsid protein is sufficient for attenuation in vivo. J. Virol 2008, 82, 7725–7728.
[22]  Bruggink, L; Marshall, J. Molecular changes in the norovirus polymerase gene and their association with incidence of GII.4 norovirus-associated gastroenteritis outbreaks in Victoria, Australia, 2001–2005. Arch. Virol 2008, 153, 729–732.
[23]  Bruggink, LD; Marshall, JA. Identification of a novel codon in the norovirus GII.4 polymerase region which acts as a marker of major GII.4 norovirus epidemics. Infect. Genet. Evol 2009, 9, 653–655.
[24]  Bull, RA; Eden, JS; Rawlinson, WD; White, PA. Rapid evolution of pandemic noroviruses of the GII.4 lineage. PLoS Pathogens 2010, 6, e1000831.
[25]  Bull, RA; Tu, ETV; McIver, CJ; Rawlinson, WD; White, PA. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J. Clin. Microbiol 2006, 44, 327–333.
[26]  Gallimore, CI; Iturriza-Gomara, M; Xerry, J; Adigwe, J; Gray, JJ. Inter-seasonal diversity of norovirus genotypes: Emergence and selection of virus variants. Arch. Virol 2007, 152, 1295–1303.
[27]  Siebenga, J; Kroneman, A; Vennema, H; Duizer, E; Koopmans, M. Food-borne viruses in Europe network report: the norovirus GII.4 2006b (for US named Minerva-like, for Japan Kobe034-like, for UK v6) variant now dominant in early seasonal surveillance. Euro Surveill 2008, 13. pii=8009.
[28]  Kroneman, A; Vennema, H; van Duijnhoven, Y; Duizer, E; Koopmans, M. High number of norovirus outbreaks associated with a GGII.4 variant in the Netherlands and elsewhere: Does this herald a worldwide increase? Euro Surveill 2004, 8. pii=2606.
[29]  Ho, ECM; Cheng, PKC; Lau, AWL; Wong, AH; Lim, WWL. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J. Clin. Microbiol 2007, 45, 2205–2211.
[30]  Oliver, B; Ng, S; Marshall, J; Greenberg, H; Gust, ID; Cresswell, V; Ward, B; Kennett, M; Birch, C. Prolonged outbreak of Norwalk gastroenteritis in an isolated guest house. Med. J. Aust 1985, 142, 391–395.
[31]  Marks, PJ; Vipond, IB; Regan, FM; Wedgwood, K; Fey, RE; Caul, EO. A school outbreak of Norwalk-like virus: Evidence for airborne transmission. Epidemiol. Infect 2003, 131, 727–736.
[32]  Marshall, JA; Dimitriadis, A; Wright, PJ. Molecular and epidemiological features of norovirus-associated gastroenteritis outbreaks in Victoria, Australia in 2001. J. Med. Virol 2005, 75, 321–331.
[33]  Bruggink, L; Sameer, R; Marshall, J. Molecular and epidemiological characteristics of norovirus associated with community-based sporadic gastroenteritis incidents and norovirus outbreaks in Victoria, Australia, 2002–2007. Intervirology 2010, 53, 167–172.
[34]  Parashar, UD; Dow, L; Fankhauser, RL; Humphrey, CD; Miller, J; Ando, T; Williams, KS; Eddy, CR; Noel, JS; Ingram, T; et al. An outbreak of viral gastroenteritis associated with consumption of sandwiches: Implications for the control of transmission by food handlers. Epidemiol. Infect 1998, 121, 615–621.
[35]  Marshall, JA; Salamone, S; Yuen, L; Catton, MG; Wright, PJ. High level excretion of Norwalk-like virus following resolution of clinical illness. Pathology 2001, 33, 50–52.
[36]  Goller, JL; Dimitriadis, A; Tan, A; Kelly, H; Marshall, JA. Long-term features of norovirus gastroenteritis in the elderly. J. Hosp. Infect 2004, 58, 286–291.
[37]  Graham, DY; Jiang, X; Tanaka, T; Opekun, AR; Madore, HP; Estes, MK. Norwalk virus infection of volunteers: New insights based on improved assays. J. Infect. Dis 1994, 170, 34–43.
[38]  Marshall, JA; Hellard, ME; Sinclair, MI; Fairley, CK; Cox, BJ; Catton, MG; Kelly, H; Wright, PJ. Failure to detect norovirus in a large group of asymptomatic individuals. Public Health 2004, 118, 230–233.
[39]  Garcia, C; DuPont, HL; Long, KZ; Santos, JI; Ko, G. Asymptomatic norovirus infection in Mexican children. J. Clin. Microbiol 2006, 44, 2997–3000.
[40]  Okabayashi, T; Yokota, S; Ohkoshi, Y; Ohuchi, H; Yoshida, Y; Kikuchi, M; Yano, K; Fujii, N. Occurrence of norovirus infections unrelated to norovirus outbreaks in an asymptomatic food handler population. J. Clin. Microbiol 2008, 46, 1985–1988.
[41]  Tu, ETV; Bull, RA; Kim, MJ; McIver, CJ; Heron, L; Rawlinson, WD; White, PA. Norovirus excretion in an aged-care setting. J. Clin. Microbiol 2008, 46, 2119–2121.
[42]  Gallimore, CI; Lewis, D; Taylor, C; Cant, A; Gennery, A; Gray, JJ. Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH). J. Clin. Virol 2004, 30, 196–204.
[43]  Henke-Gendo, C; Harste, G; Juergens-Saathoff, B; Mattner, F; Deppe, H; Heim, A. New real-time PCR detects prolonged norovirus excretion in highly immunosuppressed patients and children. J. Clin. Microbiol 2009, 47, 2855–2862.
[44]  Westhoff, TH; Vergoulidou, M; Loddenkemper, C; Schwartz, S; Hofmann, J; Schneider, T; Zidek, W; van der Giet, M. Chronic norovirus infection in renal transplant recipients. Nephrol. Dial. Transplant 2009, 24, 1051–1053.
[45]  Koopmans, M. Progress in understanding norovirus epidemiology. Curr. Opin. Infect. Dis 2008, 21, 544–552.
[46]  Doultree, JC; Druce, JD; Birch, CJ; Bowden, DS; Marshall, JA. Inactivation of feline calicivirus, a Norwalk virus surrogate. J. Hosp. Infect 1999, 41, 51–57.
[47]  Bae, J; Schwab, KJ. Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and ground water. Appl. Environ. Microbiol 2008, 74, 477–484.
[48]  Lamhoujeb, S; Fliss, I; Ngazoa, SE; Jean, J. Molecular study of the persistence of infectious human norovirus on food-contact surfaces. Food Environ. Virol 2009, 1, 51–56.
[49]  Lay, MK; Atmar, RL; Guix, S; Bharadwaj, U; He, H; Neill, FH; Sastry, KJ; Yao, Q; Estes, MK. Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology 2010, 406, 1–11.
[50]  Mounts, AW; Ando, T; Koopmans, M; Bresee, JS; Noel, J; Glass, RI. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J Infect Dis 2000, 181(Suppl 2), S284–S287.
[51]  Nygard, K; Torven, M; Ancker, C; Knauth, SB; Hedlund, KO; Giesecke, J; Andersson, Y; Svensson, L. Emerging genotype (GGIIb) of norovirus in drinking water, Sweden. Emerg. Infect. Dis 2003, 9, 1548–1552.
[52]  Hewitt, J; Bell, D; Simmons, GC; Rivera-Aban, M; Wolf, S; Greening, GE. Gastroenteritis outbreak caused by waterborne norovirus at a New Zealand ski resort. Appl. Environ. Microbiol 2007, 73, 7853–7857.
[53]  Bruggink, LD; Marshall, JA. The incidence of norovirus-associated gastroenteritis outbreaks in Victoria, Australia (2002–2007) and their relationship with rainfall. Int. J. Environ. Res. Public Health 2010, 7, 2822–2827.
[54]  Wang, QH; Han, MG; Cheetham, S; Souza, M; Funk, JA; Saif, LJ. Porcine noroviruses related to human noroviruses. Emerg. Infect. Dis 2005, 11, 1874–1881.
[55]  Wolf, S; Williamson, W; Hewitt, J; Lin, S; Rivera-Aban, M; Ball, A; Scholes, P; Savill, M; Greening, GE. Molecular detection of norovirus in sheep and pigs in New Zealand farms. Vet. Microbiol 2009, 133, 184–189.
[56]  Wobus, CE; Thackray, LB; Virgin, HW. Murine norovirus: A model system to study norovirus biology and pathogenesis. J. Virol 2006, 80, 5104–5112.
[57]  Martella, V; Lorusso, E; Decaro, N; Elia, G; Radogna, A; D’Abramo, M; Desario, C; Cavalli, A; Corrente, M; Camero, M; Germinario, CA; Banyai, K; Di Martino, B; Marsilio, F; Carmichael, LE; Buonavoglia, C. Detection and molecular characterization of a canine norovirus. Emerg. Infect. Dis 2008, 14, 1306–1308.
[58]  Martella, V; Decaro, N; Lorusso, E; Radogna, A; Moschidou, P; Amorisco, F; Lucente, MS; Desario, C; Mari, V; Elia, G; Banyai, K; Carmichael, LE; Buonavoglia, C. Genetic heterogeneity and recombination in canine noroviruses. J. Virol 2009, 83, 11391–11396.
[59]  Mesquita, JR; Barclay, L; Nascimento, MSJ; Vinje, J. Novel norovirus in dogs with diarrhea. Emerg. Infect. Dis 2010, 16, 980–982.
[60]  Ntafis, V; Xylouri, E; Radogna, A; Buonavoglia, C; Martella, V. Outbreak of canine norovirus infection in young dogs. J. Clin. Microbiol 2010, 48, 2605–2608.
[61]  Martella, V; Campolo, M; Lorusso, E; Cavicchio, P; Camero, M; Bellacicco, AL; Decaro, N; Elia, G; Greco, G; Corrente, M; Desario, C; Arista, S; Banyai, K; Koopmans, M; Buonavoglia, C. Norovirus in captive lion cub (Panthera leo). Emerg. Infect. Dis 2007, 13, 1071–1073.
[62]  Mattison, K; Shukla, A; Cook, A; Pollari, F; Friendship, R; Kelton, D; Bidawid, S; Farber, JM. Human noroviruses in swine and cattle. Emerg. Infect. Dis 2007, 13, 1184–1188.


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