Advertisement
Review Article| Volume 35, ISSUE 2, P345-362, June 2015

Laboratory Diagnosis of Noroviruses

Present and Future
  • Xiaoli Pang
    Correspondence
    Corresponding author. Provincial Laboratory for Public Health, Walter Mackenzie Health Sciences Centre, University of Alberta Hospital, 8440 - 112 Street, Edmonton, Alberta T6G 2J2, Canada.
    Affiliations
    Provincial Laboratory for Public Health, Walter Mackenzie Health Sciences Centre, University of Alberta Hospital, 8440 - 112 Street, Edmonton, Alberta T6G 2J2, Canada

    Department of Laboratory Medicine and Pathology, University of Alberta, 8440-112 Street, Edmonton, Alberta T6G 2B7, Canada
    Search for articles by this author
  • Bonita E. Lee
    Affiliations
    Department of Pediatrics, University of Alberta, 11405, 87 Avenue, Edmonton, Alberta T6G 1C9, Canada
    Search for articles by this author
Published:April 04, 2015DOI:https://doi.org/10.1016/j.cll.2015.02.008

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Siebenga J.J.
        • Vennema H.
        • Zheng D.P.
        • 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
        • Ahmed S.M.
        • Hall A.J.
        • Robinson A.E.
        • et al.
        Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis.
        Lancet Infect Dis. 2014; 14: 725-730
        • Patel M.M.
        • Widdowson M.A.
        • Glass R.I.
        • et al.
        Systematic literature review of role of noroviruses in sporadic gastroenteritis.
        Emerg Infect Dis. 2008; 4: 1224-1231
        • Payne D.C.
        • Vinjé J.
        • Szilagyi P.G.
        • et al.
        Norovirus and medically attended gastroenteritis in U.S. children.
        N Engl J Med. 2013; 368: 1121-1130
        • Bucardo F.
        • Reyes Y.
        • Svensson L.
        • et al.
        Predominance of norovirus and sapovirus in Nicaragua after implementation of universal rotavirus vaccination.
        PLoS One. 2014; 9: e98201
        • Kapikian A.Z.
        • Wyatt R.G.
        • Dolin R.
        • et al.
        Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis.
        J Virol. 1972; 10: 1075-1081
        • Tan M.
        • Jiang X.
        Norovirus P particle: a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus.
        Nanomedicine. 2012; 7: 889-897
        • Debbink K.
        • Costantini V.
        • Swanstrom J.
        • et al.
        Human norovirus detection and production, quantification, and storage of virus-like particles.
        Curr Protoc Microbiol. 2013; 31: 15
        • Green Y.K.
        Caliciviridae: the noroviruses.
        in: Knipe D.M. Howley P.M. Griffin D.E. Fields virology. 5th edition. Lippincott Williams & Wilkins, Philadelphia2007: 949-979
        • Jiang X.
        • Wang M.
        • Wang K.
        • et al.
        Sequence and genomic organization of Norwalk virus.
        Virology. 1993; 195: 51-61
        • Zheng D.P.
        • Ando T.
        • Fankhauser R.L.
        • et al.
        Norovirus classification and proposed strain nomenclature.
        Virology. 2006; 346: 312-323
        • Menon V.K.
        • George S.
        • Shanti A.A.
        • et al.
        Exposure to human and bovine noroviruses in a birth cohort in southern India from 2002 to 2006.
        J Clin Microbiol. 2013; 51: 2391-2395
        • Bruggink L.D.
        • Oluwatoyin O.
        • Sameer R.
        • et al.
        Molecular and epidemiological features of gastroenteritis outbreaks involving genogroup I norovirus in Victoria, Australia, 2002-2010.
        J Med Virol. 2012; 84: 1437-1448
        • Hoa Tran T.N.
        • Trainor E.
        • Nakagomi T.
        • et al.
        Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants.
        J Clin Virol. 2013; 56: 185-193
        • Vinjé J.
        Advances in laboratory methods for detection and typing of norovirus.
        J Clin Microbiol. 2015; 53: 373-381
        • Bull R.A.
        • Eden J.S.
        • Rawlinson W.D.
        • et al.
        Rapid evolution of pandemic noroviruses of the GII.4 lineage.
        PLoS Pathog. 2010; 6: e1000831
        • Lee B.E.
        • Preiksaitis J.K.
        • Chui N.
        • et al.
        Genetic relatedness of noroviruses identified in sporadic gastroenteritis in children and gastroenteritis outbreaks in northern Alberta.
        J Med Virol. 2008; 80: 330-337
        • Glass R.I.
        • Parashar U.D.
        • Estes M.K.
        Norovirus gastroenteritis.
        N Engl J Med. 2009; 361: 1776-1785
        • Huang P.
        • Farkas T.
        • Zhong W.
        • et al.
        Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns.
        J Virol. 2005; 79: 6714-6722
        • Krones E.
        • Högenauer C.
        Diarrhea in the immunocompromised patient.
        Gastroenterol Clin North Am. 2012; 41: 677-701
        • Bok K.
        • Green K.Y.
        Norovirus gastroenteritis in immunocompromised patients.
        N Engl J Med. 2012; 367: 2126-2132
        • Long S.S.
        Evidence of norovirus causing necrotizing enterocolitis (NEC) in a NICU.
        J Pediatr. 2008; 153: A2
        • Turcios-Ruiz R.M.
        • Axelrod P.
        • St. John K.
        • et al.
        Outbreak of necrotizing enterocolitis caused by norovirus in a neonatal intensive care unit.
        J Pediatr. 2008; 153: 339-344
        • Atmar R.L.
        • Bernstein D.I.
        • Harro C.D.
        • et al.
        Norovirus vaccine against experimental human Norwalk virus illness.
        N Engl J Med. 2011; 365: 2178-2187
        • Atmar R.L.
        • Opekun A.R.
        • Gilger M.A.
        • et al.
        Determination of the 50% human infectious dose for Norwalk virus.
        J Infect Dis. 2014; 209: 1016-1022
        • Arvelo W.
        • Hall A.J.
        • Estevez A.
        • et al.
        Diagnostic performance of rectal swab versus bulk stool specimens for the detection of rotavirus and norovirus: implications for outbreak investigations.
        J Clin Virol. 2013; 58: 678-682
        • Sidler J.A.
        • Käch R.
        • Noppen C.
        • et al.
        Rectal swab for detection of norovirus by real-time PCR: similar sensitivity compared to faecal specimens.
        Clin Microbiol Infect. 2014; 20: O1017-O1019
        • Ito S.
        • Takeshita S.
        • Nezu A.
        • et al.
        Norovirus-associated encephalopathy.
        Pediatr Infect Dis J. 2006; 25: 651-652
        • Takanashi S.
        • Hashira S.
        • Matsunaga T.
        • et al.
        Detection, genetic characterization, and quantification of norovirus RNA from sera of children with gastroenteritis.
        J Clin Virol. 2009; 44: 161-163
        • Fumian T.M.
        • Justino M.C.
        • D'Arc Pereira Mascarenhas J.
        • et al.
        Quantitative and molecular analysis of noroviruses RNA in blood from children hospitalized for acute gastroenteritis in Belém, Brazil.
        J Clin Virol. 2013; 58: 31-35
        • Medici M.C.
        • Abelli L.A.
        • Dodi I.
        • et al.
        Norovirus RNA in the blood of a child with gastroenteritis and convulsions – a case report.
        J Clin Virol. 2010; 48: 147-149
        • Duizer E.
        • Pielaat A.
        • Vennema H.
        • et al.
        Probabilities in norovirus outbreak diagnosis.
        J Clin Virol. 2007; 40: 38-42
        • Pang X.L.
        • Preiksaitis J.K.
        • Wong S.
        • et al.
        Influence of novel norovirus GII.4 variants on gastroenteritis outbreak dynamics in Alberta and the Northern Territories, Canada between 2000 and 2008.
        PLoS One. 2010; 5: e11599
        • Pang X.L.
        • Preiksaitis J.K.
        • Lee B.E.
        Enhanced enteric virus detection in sporadic gastroenteritis using a multi-target real-time PCR panel – a one-year study.
        J Med Virol. 2014; 86: 1594-1601
        • Richards A.F.
        • Lopman B.
        • Gunn A.
        • et al.
        Evaluation of a commercial ELISA for detecting Norwalk-like virus antigen in faeces.
        J Clin Virol. 2003; 26: 109-115
        • Burton-MacLeod J.A.
        • Kane E.M.
        • Beard R.S.
        • et al.
        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
        • Gray J.J.
        • Kohli E.
        • Ruggeri F.M.
        • et al.
        European multicenter evaluation of commercial enzyme immunoassays for detecting norovirus antigen in fecal samples.
        Clin Vaccine Immunol. 2007; 14: 1349-1355
        • Takanashi S.
        • Okame M.
        • Shiota T.
        • et al.
        Development of a rapid immunochromatographic test for noroviruses genogroups I and II.
        J Virol Methods. 2008; 148: 1-8
        • Khamrin P.
        • Nguyen T.A.
        • Phan T.G.
        • et al.
        Evaluation of immunochromatography and commercial enzyme-linked immunosorbent assay for rapid detection of norovirus antigen in stool samples.
        J Virol Methods. 2008; 147: 360-363
        • Derrington P.
        • Schreiber F.
        • Day S.
        • et al.
        Norovirus Ridaquick: a new test for rapid diagnosis of norovirus.
        Pathology. 2009; 41: 687-688
        • Bruins M.J.
        • Wolfhagen M.J.
        • Schirm J.
        • et al.
        Evaluation of a rapid immunochromatographic test for the detection of norovirus in stool samples.
        Eur J Clin Microbiol Infect Dis. 2010; 29: 741-743
        • Kirby A.
        • Gurgel R.Q.
        • Dove W.
        • et al.
        An evaluation of the RIDASCREEN and IDEIA enzyme immunoassays and the RIDAQUICK immunochromatographic test for the detection of norovirus in faecal specimens.
        J Clin Virol. 2010; 49: 254-257
        • Bruggink L.D.
        • Witlox K.J.
        • Sameer R.
        • et al.
        Evaluation of the RIDA®QUICK immunochromatographic norovirus detection assay using specimens from Australian gastroenteritis incidents.
        J Virol Methods. 2011; 173: 121-126
        • Geginat G.
        • Kaiser D.
        • Schrempf S.
        Evaluation of third-generation ELISA and a rapid immunochromatographic assay for the detection of norovirus infection in fecal samples from inpatients of a German tertiary care hospital.
        Eur J Clin Microbiol Infect Dis. 2012; 31: 733-737
        • Thongprachum A.
        • Khamrin P.
        • Tran D.N.
        • et al.
        Evaluation and comparison of the efficiency of immunochromatography methods for norovirus detection.
        Clin Lab. 2012; 58: 489-493
        • Sakamaki N.
        • Ohiro Y.
        • Ito M.
        • et al.
        Bioluminescent enzyme immunoassay for the detection of norovirus capsid antigen.
        Clin Vaccine Immunol. 2012; 19: 1949-1954
        • Ambert-Balay K.
        • Pothier P.
        Evaluation of 4 immunochromatographic tests for rapid detection of norovirus in faecal samples.
        J Clin Virol. 2013; 56: 194-198
        • Shigemoto N.
        • Tanizawa Y.
        • Matsuo T.
        • et al.
        Clinical evaluation of a bioluminescent enzyme immunoassay for detecting norovirus in fecal specimens from patients with acute gastroenteritis.
        J Med Virol. 2014; 86: 1219-1225
        • Dunbar S.A.
        • Zhang H.
        • Tang Y.W.
        Advanced techniques for detection and identification of microbial agents of gastroenteritis.
        Clin Lab Med. 2013; 33: 527-552
        • Rasool N.B.
        • Monroe S.S.
        • Glass R.I.
        Determination of a universal nucleic acid extraction procedure for PCR detection of gastroenteritis viruses in faecal specimens.
        J Virol Methods. 2002; 100: 1-16
        • Al-Soud W.A.
        • Radstrom P.
        Purification and characterization of PCR-inhibitory components in blood cells.
        J Clin Microbiol. 2001; 39: 485-493
        • Jiang X.
        • Wang J.
        • Graham D.Y.
        • et al.
        Detection of Norwalk virus in stool by polymerase chain reaction.
        J Clin Microbiol. 1992; 30: 2529-2534
        • Mattison K.
        • Grudeski E.
        • Auk B.
        • et al.
        Multicenter comparison of two norovirus ORF2-based genotyping protocols.
        J Clin Microbiol. 2009; 47: 3927-3932
        • Kageyama T.
        • Kojima S.
        • Shinohara M.
        • et al.
        Broadly reactive and highly sensitive assay for norwalk-like viruses based on real-time quantitative reverse transcription-PCR.
        J Clin Microbiol. 2003; 41: 1548-1557
        • Pang X.L.
        • Preiksaitis J.K.
        • Lee B.
        Multiplex real time RT-PCR for the detection and quantitation of norovirus genogroups I and II in patients with acute gastroenteritis.
        J Clin Virol. 2005; 33: 168-171
        • Trujillo A.A.
        • McCaustland K.A.
        • Zheng D.P.
        • et al.
        Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus.
        J Clin Microbiol. 2006; 44: 1405-1412
        • Hoehne M.
        • Schreier E.
        Detection of Norovirus genogroup I and II by multiplex real-time RT-PCR using a 3'-minor groove binder-DNA probe.
        BMC Infect Dis. 2006; https://doi.org/10.1186/1471-2334-6-69
        • Jothikumar N.
        • Lowther J.A.
        • Henshilwood K.
        • et al.
        Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples.
        Appl Environ Microbiol. 2005; 71: 1870-1875
        • Logan C.L.
        • O'Leary J.J.
        • O'Sullivan N.
        Real-time reverse transcription PCR detection of norovirus, sapovirus and astrovirus as causative agents of acute viral gastroenteritis.
        J Virol Methods. 2007; 146: 36-44
        • Stals A.
        • Baert L.
        • Botteldoorn N.
        • et al.
        Multiplex real-time RT-PCR for simultaneous detection of GI/GII noroviruses and murine norovirus 1.
        J Virol Methods. 2009; 161: 247-253
        • Neesanant P.
        • Sirinarumitr T.
        • Chantakru S.
        • et al.
        Optimization of one-step real-time reverse transcription-polymerase chain reaction assays for norovirus detection and molecular epidemiology of noroviruses in Thailand.
        J Virol Methods. 2013; 194: 317-325
        • Butot S.
        • Le Guyader F.S.
        • Krol J.
        • et al.
        Evaluation of various real-time RT-PCR assays for the detection and quantitation of human norovirus.
        J Virol Methods. 2010; 167: 90-94
        • Moore C.
        • Clark E.M.
        • Gallimore C.I.
        • et al.
        Evaluation of a broadly reactive nucleic acid sequence based amplification assay for the detection of noroviruses in faecal material.
        J Clin Virol. 2004; 29: 290-296
        • Notomi T.
        • Okayama H.
        • Masubuchi H.
        • et al.
        Loop-mediated isothermal amplification of DNA.
        Nucleic Acids Res. 2000; 28: E63
        • Iturriza-Gómara M.
        • Xerry J.
        • Gallimore C.I.
        • et al.
        Evaluation of the Loopamp (loop-mediated isothermal amplification) kit for detecting norovirus RNA in faecal samples.
        J Clin Virol. 2008; 42: 389-393
        • Yoda T.
        • Suzuki Y.
        • Yamazaki Y.
        • et al.
        Application of a modified loop-mediated isothermal amplification kit for detecting norovirus genogroups I and II.
        J Med Virol. 2009; 81: 2072-2078
        • Suzuki Y.
        • Narimatsu S.
        • Furukawa T.
        • et al.
        Comparison of real-time reverse-transcription loop-mediated isothermal amplification and real-time reverse-transcription polymerase chain reaction for detection of noroviruses in municipal wastewater.
        J Biosci Bioeng. 2011; 112: 369-372
        • Navidad J.F.
        • Griswold D.J.
        • Gradus M.S.
        • et al.
        Evaluation of Luminex xTAG gastrointestinal pathogen analyte-specific reagents for high-throughput, simultaneous detection of bacteria, viruses, and parasites of clinical and public health importance.
        J Clin Microbiol. 2013; 51: 3018-3024
        • Mengelle C.
        • Mansuy J.M.
        • Prere M.F.
        • et al.
        Simultaneous detection of gastrointestinal pathogens with a multiplex Luminex-based molecular assay in stool samples from diarrhoeic patients.
        Clin Microbiol Infect. 2013; 19: E458-E465
        • Claas E.
        • Burnham C.A.
        • Mazulli T.
        • et al.
        Performance of the xTAG® Gastrointestinal Pathogen Panel (GPP), a multiplex molecular assay for simultaneous detection of bacterial, viral and parasitic causes of infectious gastroenteritis.
        J Microbiol Biotechnol. 2013; 23: 1041-1045
        • Khare R.
        • Espy M.J.
        • Cebelinski E.
        • et al.
        Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens.
        J Clin Microbiol. 2014; 52: 3667-3673
        • Hasing M.E.
        • Hazes B.
        • Lee B.E.
        • et al.
        Detection and analysis of recombination in GII.4 norovirus strains causing gastroenteritis outbreaks in Alberta.
        Infect Genet Evol. 2014; 27: 181-192
        • Srivatsan A.
        • Han Y.
        • Peng J.
        • et al.
        High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies.
        PLoS Genet. 2008; 4: e1000139
        • Rasmussen M.
        • Li Y.
        • Lindgreen S.
        • et al.
        Ancient human genome sequence of an extinct Palaeo-Eskimo.
        Nature. 2010; 463: 757-762
        • Lo Y.M.
        • Chiu R.W.
        Next-generation sequencing of plasma/serum DNA: an emerging research and molecular diagnostic tool.
        Clin Chem. 2009; 55: 607-608
        • Wong T.H.
        • Dearlove B.L.
        • Hedge J.
        • et al.
        Whole genome sequencing and de novo assembly identifies Sydney-like variant noroviruses and recombinants during the winter 2012/2013 outbreak in England.
        Virol J. 2013; 10: 335
        • Batty E.M.
        • Wong T.H.
        • Trebes A.
        • et al.
        A modified RNA-Seq approach for whole genome sequencing of RNA viruses from faecal and blood samples.
        PLoS One. 2013; 8: e66129
        • Kundu S.
        • Lockwood J.
        • Depledge D.P.
        • et al.
        Next-generation whole genome sequencing identifies the direction of norovirus transmission in linked patients.
        Clin Infect Dis. 2013; 57: 407-414
        • Cotten M.
        • Petrova V.
        • Phan M.V.
        • et al.
        Deep sequencing of norovirus genomes defines evolutionary patterns in an urban tropical setting.
        J Virol. 2014; 88: 11056-11069