Serogrouping and seroepidemiology of North European hantaviruses using a novel broadly targeted synthetic nucleoprotein antigen array

References

• Vaheri A , Henttonen H , Voutilainen L , et al. Hantavirus infections in Europe and their impact on public health. Rev Med Virol. 2013;23:1–11.
   Web of Science ®Google Scholar
• Holmes EC , Zhang Y-Z. The evolution and emergence of hantaviruses. Curr Opin Virol. 2015;10:27–33.
   PubMed Web of Science ®Google Scholar
• Heyman P , Vervoort T , Colson P , et al. A major outbreak of hantavirus infection in Belgium in 1995 and 1996. Epidemiol Infect. 1999;122:447–453.
   PubMed Web of Science ®Google Scholar
• Heyman P , Plyusnina A , Berny P , et al. Seoul hantavirus in Europe: first demonstration of the virus genome in wild Rattus norvegicus captured in France. Eur J Clin Microbiol Infect Dis. 2004;23:711–717.
   PubMed Web of Science ®Google Scholar
• Heyman P , Baert K , Plyusnina A , et al. Serological and genetic evidence for the presence of seoul hantavirus in Rattus norvegicus in Flanders, Belgium. Scand J Infect Dis. 2009;41:51–56.
   PubMed Web of Science ®Google Scholar
• Sanfeliu I , Nogueras MM , Gegúndez MI , et al. Seroepidemiological survey of hantavirus infection in healthy people in Valles Occidental, Barcelona. Vector Borne Zoonotic Dis. 2011;11:697–700.
   Web of Science ®Google Scholar
• Lin X-D , Guo W-P , Wang W , et al. Migration of Norway rats resulted in the worldwide distribution of Seoul hantavirus today. J Virol. 2012;86:972–981.
   PubMed Web of Science ®Google Scholar
• Plyusnina A , Heyman P , Baert K , et al. Genetic characterization of Seoul hantavirus originated from Norway rats (Rattus norvegicus) captured in Belgium. J Med Virol. 2012;84:1298–1303.
   Web of Science ®Google Scholar
• Clement J , Maes P , Van Ranst M. Hemorrhagic fever with renal syndrome in the new, and hantavirus pulmonary syndrome in the old world: paradi(se)gm lost or regained? Virus Res. 2014;187:55–58.
   PubMed Web of Science ®Google Scholar
• Christova I , Plyusnina A , Gladnishka T , et al. Detection of Dobrava hantavirus RNA in apodemus mice in Bulgaria. J Med Virol. 2015;87:263–268.
   Web of Science ®Google Scholar
• Goeijenbier M , Verner-Carlsson J , van Gorp EC , et al. Seoul hantavirus in brown rats in the Netherlands: implications for physicians – epidemiology, clinical aspects, treatment and diagnostics. Neth J Med. 2015;73:155–160.
   Web of Science ®Google Scholar
• Verner-Carlsson J , Lohmus M , Sundstrom K , et al. First evidence of Seoul hantavirus in the wild rat population in the Netherlands. Infect Ecol Epidemiol. 2015;5:27215.
   Google Scholar
• Avsic-Zupanc T , Petrovec M , Duh D , et al. Puumala hantavirus in Slovenia: analyses of S and M segment sequences recovered from patients and rodents. Virus Res. 2007;123:204–210.
   Web of Science ®Google Scholar
• Voutilainen L , Sironen T , Tonteri E , et al. Life-long shedding of Puumala hantavirus in wild bank voles (Myodes glareolus). J Gen Virol. 2015;96:1238–1247.
   PubMed Web of Science ®Google Scholar
• Watson DC , Sargianou M , Papa A , et al. Epidemiology of hantavirus infections in humans: a comprehensive, global overview. Crit Rev Microbiol. 2014;40:261–272.
   PubMed Web of Science ®Google Scholar
• Manigold T , Vial P . Human hantavirus infections: epidemiology, clinical features, pathogenesis and immunology. Swiss Med Wkly. 2014;144:w13937.
   PubMed Web of Science ®Google Scholar
• Reusken C , Heyman P . Factors driving hantavirus emergence in Europe. Curr Opin Virol. 2013;3:92–99.
   PubMed Web of Science ®Google Scholar
• Hartline J , Mierek C , Knutson T , et al. Hantavirus infection in North America: a clinical review. Am J Emerg Med. 2013;31:978–982.
   Web of Science ®Google Scholar
• Mattar S , Guzmán C , Figueiredo LT . Diagnosis of hantavirus infection in humans. Expert Rev Anti Infect Ther. 2015;13:939–946.
   PubMed Web of Science ®Google Scholar
• Lundkvist A , Meisel H , Koletzki D , et al. Mapping of B-cell epitopes in the nucleocapsid protein of Puumala hantavirus. Viral Immunol. 2002;15:177–192.
   Web of Science ®Google Scholar
• Heiskanen T , Lundkvist A , Soliymani R , et al. Phage-displayed peptides mimicking the discontinuous neutralization sites of Puumala hantavirus envelope glycoproteins. Virology. 1999;262:321–332.
   Web of Science ®Google Scholar
• Elfaitouri A , Herrmann B , Bolin-Wiener A , et al. Epitopes of microbial and human heat shock protein 60 and their recognition in myalgic encephalomyelitis. PLoS One. 2013;8:e81155.
   Web of Science ®Google Scholar
• Blomberg J , Blomberg F , Sjösten A , et al. No evidence for xenotropic murine leukemia-related virus infection in Sweden using internally controlled multiepitope suspension array serology. Clin Vaccine Immunol. 2012;19:1399–1410.
   PubMed Web of Science ®Google Scholar
• Rizwan M , Ronnberg B , Cistjakovs M , et al. Serology in the digital age: using long synthetic peptides created from nucleic acid sequences as antigens in microarrays. Microarrays (Basel). 2016;5.
   Google Scholar
• Elgh F , Linderholm M , Wadell G , et al. Development of humoral cross-reactivity to the nucleocapsid protein of heterologous hantaviruses in nephropathia epidemica. FEMS Immunol Med Microbiol. 1998;22:309–315.
   PubMedGoogle Scholar
• Yoshimatsu K , Arikawa J . Serological diagnosis with recombinant N antigen for hantavirus infection. Virus Res. 2014;187:77–83.
   PubMed Web of Science ®Google Scholar
• Yoshimatsu K , Arikawa J . Antigenic properties of N protein of hantavirus. Viruses. 2014;6:3097–3109.
   PubMed Web of Science ®Google Scholar
• Zhang Q , Wang P , Kim Y , et al. Immune epitope database analysis resource (IEDB-AR). Nucleic Acids Res. 2008;36:W513–W518.
   PubMed Web of Science ®Google Scholar
• Wang Y , Boudreaux DM , Estrada DF , et al. NMR structure of the N-terminal coiled coil domain of the Andes hantavirus nucleocapsid protein. J Biol Chem. 2008;283:28297–28304.
   Web of Science ®Google Scholar
• Goeijenbier M , Hartskeerl RA , Reimerink J , et al. The hanta hunting study: underdiagnosis of Puumala hantavirus infections in symptomatic non-travelling leptospirosis-suspected patients in the Netherlands, in 2010 and April to November 2011. Euro Surveill. 2014;19:20878.
   Google Scholar
• Gherasim A , Hjertqvist M , Lundkvist A , et al. Risk factors and potential preventive measures for nephropatia epidemica in Sweden 2011–2012: a case-control study. Infect Ecol Epidemiol. 2015;5:27698.
   PubMedGoogle Scholar
• Lundkvist A , Kallio-Kokko H , Sjölander KB , et al. Characterization of Puumala virus nucleocapsid protein: identification of B-cell epitopes and domains involved in protective immunity. Virology. 1996;216:397–406.
   PubMed Web of Science ®Google Scholar
• Kallio-Kokko H , Leveelahti R , Brummer-Korvenkontio M , et al. Human immune response to Puumala virus glycoproteins and nucleocapsid protein expressed in mammalian cells. J Med Virol. 2001;65:605–613.
   PubMed Web of Science ®Google Scholar
• Hedman K , Vaheri A , Brummer-Korvenkontio M . Rapid diagnosis of hantavirus disease with an igg-avidity assay. Lancet. 1991;338:1353–1356.
   PubMed Web of Science ®Google Scholar
• Sjölander KB , Elgh F , Kallio-Kokko H , et al. Evaluation of serological methods for diagnosis of Puumala hantavirus infection (nephropathia epidemica). J Clin Microbiol. 1997;35:3264–3268.
   PubMed Web of Science ®Google Scholar
• Hepojoki S , Rusanen J , Hepojoki J , et al. Competitive homogeneous immunoassay for rapid serodiagnosis of hantavirus disease. J Clin Microbiol. 2015;53:2292–2297.
   Web of Science ®Google Scholar
• Klingström J , Plyusnin A , Vaheri A , et al. Wild-type Puumala hantavirus infection induces cytokines, C-reactive protein, creatinine, and nitric oxide in cynomolgus macaques. J Virol. 2002;76:444–449.
   PubMed Web of Science ®Google Scholar
• Lohmus M , Verner-Carlsson J , Borg O , et al. Hantavirus in new geographic regions, Sweden. Infect Ecol Epidemiol. 2016;6:31465.
   Google Scholar
• Haste Andersen P , Nielsen M , Lund O . Prediction of residues in discontinuous B-cell epitopes using protein 3D structures. Protein Sci. 2006;15:2558–2567.
   PubMed Web of Science ®Google Scholar
• Vapalahti O , Kallio-Kokko H , Närvänen A , et al. Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response. J Med Virol. 1995;46:293–303.
   PubMed Web of Science ®Google Scholar
• Dzagurova T , Tkachenko E , Slonova R , et al. Antigenic relationships of hantavirus strains analysed by monoclonal antibodies. Arch Virol. 1995;140:1763–1773.
   PubMed Web of Science ®Google Scholar
• Xu L , Wu J , He B , et al. Novel hantavirus identified in black-bearded tomb bats, China. Infect Genet Evol. 2015;31:158–160.
   Web of Science ®Google Scholar
• Noh JY , Cheong HJ , Song JY , et al. Clinical and molecular epidemiological features of hemorrhagic fever with renal syndrome in Korea over a 10-year period. J Clin Virol. 2013;58:11–17.
   PubMed Web of Science ®Google Scholar
• Terajima M , Hendershot JD 3rd , Kariwa H , et al. High levels of viremia in patients with the hantavirus pulmonary syndrome. J Infect Dis. 1999;180:2030–2034.
   PubMed Web of Science ®Google Scholar
• Elgh F , Lundkvist A , Alexeyev OA , et al. A major antigenic domain for the human humoral response to Puumala virus nucleocapsid protein is located at the amino-terminus. J Virol Methods. 1996;59:161–172.
   PubMed Web of Science ®Google Scholar
• de Carvalho Nicacio C , Sällberg M , Hultgren C , et al. T-helper and humoral responses to Puumala hantavirus nucleocapsid protein: identification of T-helper epitopes in a mouse model. J Gen Virol. 2001;82:129–138.
   Web of Science ®Google Scholar
• Todd DJ , Knowlton N , Amato M , et al. Erroneous augmentation of multiplex assay measurements in patients with rheumatoid arthritis due to heterophilic binding by serum rheumatoid factor. Arthritis Rheum. 2011;63:894–903.
   PubMed Web of Science ®Google Scholar
• Waterboer T , Sehr P , Pawlita M . Suppression of non-specific binding in serological luminex assays. J Immunol Methods. 2006;309:200–204.
   PubMed Web of Science ®Google Scholar
• Razzauti M , Plyusnina A , Sironen T , et al. Analysis of Puumala hantavirus in a bank vole population in northern Finland: evidence for co-circulation of two genetic lineages and frequent reassortment between strains. J Gen Virol. 2009;90:1923–1931.
   Web of Science ®Google Scholar
• Lundkvist A , Verner-Carlsson J , Plyusnina A , et al. Pet rat harbouring Seoul hantavirus in Sweden, June 2013. Euro Surveill. 2013;18:20521.
   Google Scholar
• Ling J , Vaheri A , Hepojoki S , et al. Serological survey of Seewis virus antibodies in patients suspected for hantavirus infection in Finland; a cross-reaction between Puumala virus antiserum with Seewis virus N protein? J Gen Virol. 2015;96:1664–1675.
   Web of Science ®Google Scholar