Evidence for Human Norovirus Infection of Dogs in the United Kingdom

ABSTRACT Human noroviruses (HuNoVs) are a major cause of viral gastroenteritis, with an estimated 3 million cases per year in the United Kingdom. HuNoVs have recently been isolated from pet dogs in Europe (M. Summa, C.-H. von Bonsdorff, and L. Maunula, J Clin Virol 53:244–247, 2012, http://dx.doi.org/10.1016/j.jcv.2011.12.014), raising concerns about potential zoonotic infections. With 31% of United Kingdom households owning a dog, this could prove to be an important transmission route. To examine this risk, canine tissues were studied for their ability to bind to HuNoV in vitro. In addition, canine stool samples were analyzed for the presence of viral nucleic acid, and canine serum samples were tested for the presence of anti-HuNoV antibodies. The results showed that seven different genotypes of HuNoV virus-like particles (VLPs) can bind to canine gastrointestinal tissue, suggesting that infection is at least theoretically possible. Although HuNoV RNA was not identified in stool samples from 248 dogs, serological evidence of previous exposure to HuNoV was obtained in 43/325 canine serum samples. Remarkably, canine seroprevalence for different HuNoV genotypes mirrored the seroprevalence in the human population. Though entry and replication within cells have not been demonstrated, the canine serological data indicate that dogs produce an immune response to HuNoV, implying productive infection. In conclusion, this study reveals zoonotic implications for HuNoV, and to elucidate the significance of this finding, further epidemiological and molecular investigations will be essential.

[1]  I. Clarke,et al.  Norwalk-like viruses , 2002 .

[2]  S. Dawson,et al.  Surveillance of diarrhoea in small animal practice through the Small Animal Veterinary Surveillance Network (SAVSNET). , 2014, Veterinary journal.

[3]  Marion Koopmans,et al.  Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. , 2014, The Lancet. Infectious diseases.

[4]  J. Le Pendu,et al.  Genogroup IV and VI Canine Noroviruses Interact with Histo-Blood Group Antigens , 2014, Journal of Virology.

[5]  J. Vinjé,et al.  Seroprevalence of Canine Norovirus in 14 European Countries , 2014, Clinical and Vaccine Immunology.

[6]  A. de Rougemont,et al.  Serological Evidence for Multiple Strains of Canine Norovirus in the UK Dog Population , 2013, PloS one.

[7]  J. Vinjé,et al.  Presence of Antibodies against Genogroup VI Norovirus in Humans , 2013, Virology Journal.

[8]  N. Cunliffe,et al.  Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. , 2013, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[9]  Gagandeep Kang,et al.  Comparison of Age-Stratified Seroprevalence of Antibodies against Norovirus GII in India and the United Kingdom , 2013, PloS one.

[10]  E. Thiry,et al.  A Review of Known and Hypothetical Transmission Routes for Noroviruses , 2012, Food and Environmental Virology.

[11]  J. Klena,et al.  Viral Gastroenteritis Associated with Genogroup II Norovirus among U.S. Military Personnel in Turkey, 2009 , 2012, PloS one.

[12]  J. Wain,et al.  Changes in causes of acute gastroenteritis in the United Kingdom over 15 years: microbiologic findings from 2 prospective, population-based studies of infectious intestinal disease. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[13]  D. Chao,et al.  Detection of Multiple Genotypes of Calicivirus Infection in Asymptomatic Swine in Taiwan , 2012, Zoonoses and public health.

[14]  L. Maunula,et al.  Pet dogs--a transmission route for human noroviruses? , 2012, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[15]  Qiuhong Wang,et al.  Discovery and Genomic Characterization of Noroviruses from a Gastroenteritis Outbreak in Domestic Cats in the US , 2012, PloS one.

[16]  A. Dell,et al.  Histo-Blood Group Antigens Act as Attachment Factors of Rabbit Hemorrhagic Disease Virus Infection in a Virus Strain-Dependent Manner , 2011, PLoS pathogens.

[17]  Laura C Rodrigues,et al.  Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice , 2011, Gut.

[18]  P. Pothier,et al.  Qualitative and Quantitative Analysis of the Binding of GII.4 Norovirus Variants onto Human Blood Group Antigens , 2011, Journal of Virology.

[19]  J. Vinjé,et al.  Novel Norovirus in Dogs with Diarrhea , 2010, Emerging infectious diseases.

[20]  W. Browne,et al.  Number and ownership profiles of cats and dogs in the UK , 2010, Veterinary Record.

[21]  P. Teunis,et al.  Norwalk virus: How infectious is it? , 2008, Journal of medical virology.

[22]  K. Bányai,et al.  Detection and Molecular Characterization of a Canine Norovirus , 2008, Emerging infectious diseases.

[23]  Manish M Patel,et al.  Systematic Literature Review of Role of Noroviruses in Sporadic Gastroenteritis , 2008, Emerging infectious diseases.

[24]  J. Bradshaw,et al.  Dog-human and dog-dog interactions of 260 dog-owning households in a community in Cheshire , 2008, Veterinary Record.

[25]  J. Wood,et al.  Risk of vomiting and diarrhoea in dogs , 2007, Veterinary Record.

[26]  D. Kelton,et al.  Human Noroviruses in Swine and Cattle , 2007, Emerging infectious diseases.

[27]  M. Han,et al.  Pathogenesis of a Genogroup II Human Norovirus in Gnotobiotic Pigs , 2006, Journal of Virology.

[28]  Tomoyuki N. Tanaka,et al.  Genetic and antigenic diversity among noroviruses. , 2006, The Journal of general virology.

[29]  Roger I Glass,et al.  Norovirus classification and proposed strain nomenclature. , 2006, Virology.

[30]  N. Bovin,et al.  Influence of the combined ABO, FUT2, and FUT3 polymorphism on susceptibility to Norwalk virus attachment. , 2005, The Journal of infectious diseases.

[31]  A. M. Hutson,et al.  Norwalk virus infection associates with secretor status genotyped from sera , 2005, Journal of medical virology.

[32]  E. Claas,et al.  Diagnosis of human metapneumovirus and rhinovirus in patients with respiratory tract infections by an internally controlled multiplex real-time RNA PCR , 2005, Journal of Clinical Virology.

[33]  Xi Jiang,et al.  Seroprevalence of Noroviruses in Swine , 2005, Journal of Clinical Microbiology.

[34]  Xi Jiang,et al.  Seroepidemiology and risk factors for sporadic norovirus/Mexico strain. , 2004, The Journal of infectious diseases.

[35]  M. Altaye,et al.  Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. , 2003, The Journal of infectious diseases.

[36]  Xi Jiang,et al.  Human susceptibility and resistance to Norwalk virus infection , 2003, Nature Medicine.

[37]  K. Erles,et al.  Detection of a group 2 coronavirus in dogs with canine infectious respiratory disease , 2003, Virology.

[38]  S. Fukushi,et al.  Broadly Reactive and Highly Sensitive Assay for Norwalk-Like Viruses Based on Real-Time Quantitative Reverse Transcription-PCR , 2003, Journal of Clinical Microbiology.

[39]  Benjamin A Lopman,et al.  Two Epidemiologic Patterns of Norovirus Outbreaks: Surveillance in England and Wales, 1992–2000 , 2003, Emerging infectious diseases.

[40]  A. M. Hutson,et al.  Norwalk Virus-Like Particle Hemagglutination by Binding to H Histo-Blood Group Antigens , 2003, Journal of Virology.

[41]  Harry Vennema,et al.  Natural history of human calicivirus infection: a prospective cohort study. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[42]  J. Le Pendu,et al.  Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals , 2002, Gastroenterology.

[43]  R. Glass,et al.  Characterization of Capsid Genes, Expressed in the Baculovirus System, of Three New Genetically Distinct Strains of “Norwalk-Like Viruses” , 2001, Journal of Clinical Microbiology.

[44]  J. Le Pendu,et al.  ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. , 2001, Biochimie.

[45]  J. Le Pendu,et al.  Binding of Rabbit Hemorrhagic Disease Virus to Antigens of the ABH Histo-Blood Group Family , 2000, Journal of Virology.

[46]  D. Graham,et al.  Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein , 1992, Journal of virology.

[47]  G. Amidon,et al.  Comparison of gastrointestinal pH in dogs and humans: implications on the use of the beagle dog as a model for oral absorption in humans. , 1986, Journal of pharmaceutical sciences.

[48]  T. Humphrey,et al.  An outbreak of calicivirus associated gastroenteritis in an elderly persons home. A possible zoonosis? , 1984, Journal of Hygiene.

[49]  M. Estes,et al.  Norovirus gastroenteritis. , 2009, The New England journal of medicine.

[50]  E. Thiry,et al.  Animal noroviruses. , 2008, Veterinary journal.

[51]  E. Thiry,et al.  Review of Animal Noroviruses , 2008 .

[52]  S. Nakajima,et al.  Detection of Norwalk-like virus genes in the caecum contents of pigs , 1998, Archives of Virology.