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Sindbis Virus and Pogosta Disease in Finland

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Sindbis Virus and Pogosta Disease in Finland Department of Virology Haartman Institute, Faculty of Medicine University of Helsinki SINDBIS VIRUS AND POGOSTA DISEASE IN FINLAND SATU KURKELA ACADEMIC DISSERTATION Pro Doctoratu To be presented with due permission of the Faculty of Medicine at the University of Helsinki for public examination and debate on Friday, November 23rd, 2007, at 12 noon in the Lecture Hall 3 at Biomedicum Helsinki, Haartmaninkatu 8, Helsinki HELSINKI 2007 SUPERVISORS____________________________________________________ OLLI VAPALAHTI, MD, PHD Departments of Virology and Basic Veterinary Sciences Professor of Zoonotic Virology Faculties of Medicine and Veterinary Medicine University of Helsinki Helsinki, Finland ANTTI VAHERI, MD, PHD Department of Virology Professor of Virology Faculty of Medicine University of Helsinki Helsinki, Finland REVIEWERS______________________________________________________ TYTTI VUORINEN, MD, PHD Department of Virology Docent in Virology Faculty of Medicine University of Turku Turku, Finland JARMO OKSI, MD, PHD Department of Medicine Docent in Internal Medicine Turku University Central Hospital Turku, Finland OFFICIAL OPPONENT____________________________________________ ANTOINE GESSAIN, MD, PhD Oncogenic Virus Epidemiology Head of Laboratory, Unit Chief and Pathophysiology Unit Department of Virology Institut Pasteur Paris, France Back cover art courtesy of Sini Virtanen, specially drawn for this publication ISBN 978-952-92-2880-5 (paperback) ISBN 978-952-10-4262-1 (PDF, available at http://ethesis.helsinki.fi) Yliopistopaino – Helsinki University Printing House Helsinki 2007 Your theory is crazy, but it's not crazy enough to be true - Niels Bohr (1885-1962) – CONTENTS – CONTENTS LIST OF ORIGINAL PUBLICATIONS 6 ABBREVIATIONS 7 ABSTRACT 8 TIIVISTELMÄ (SUMMARY IN FINNISH) 10 REVIEW OF THE LITERATURE 12 1. Arboviruses as human pathogens 12 2. Introduction to alphaviruses 13 Classification, genomic structure, and replication 13 Phylogenetic relationships and geographic distribution 16 Reservoirs and vectors 20 Alphaviruses as human pathogens 21 3. Clinical review of neuropathogenic alphaviruses 22 Eastern equine encephalitis virus 22 Western equine encephalitis virus 23 Venezuelan equine encephalitis virus 24 Pathogenesis of neuropathogenic alphavirus infections 25 4. Clinical review of arthritogenic alphaviruses 26 Sindbis virus 26 Ross River virus 28 Barmah Forest virus 29 Chikungunya virus 30 O’nyong-nyong virus 31 Mayaro virus 31 Pathogenesis of alphavirus arthritis 32 5. Alphavirus diagnostics, treatment, and prevention 33 6. Other arthritogenic virus infections 34 AIMS OF THE STUDY 36 MATERIALS AND METHODS 37 Patients and materials 37 Patients and patient samples (II, III, IV) 37 Serum specimen library (I, V) 39 4 SATU KURKELA - CONTENTS - Database material (V) 39 Resident grouse blood samples (V) 39 Migratory bird blood samples (V) 40 Cell lines (I, II, V) 40 Methods 40 Virus isolation (II, V) 40 RNA extraction (II, III, V) 41 Nucleic acid detection with RT-PCR (II, III, V) 41 Cloning, sequence analysis and phylogeny (II) 42 SINV IgM and IgG EIAs (I, II, III, IV, V) 43 Virus production for the EIAs 43 Coating of the EIA plates 43 IgM and IgG EIAs 43 Electron microscopy (I) 44 HI test (I, II, III, IV, V) 44 NT (I, V) 45 IFA (I, II) 45 Immunoblotting (I) 45 Immunohistochemical analysis (III) 46 RESULTS AND DISCUSSION 47 1. Serodiagnosis of SINV infection (I) 47 EIA for the serodiagnostics of SINV infection 47 Antigenic properties of the purified SINV used as EIA antigen 49 Diagnostic criteria 50 2. Etiology of Pogosta disease (II) 50 3. Clinical picture of acute Pogosta disease (III) 51 4. Prognosis of Pogosta disease (III, IV) 52 Persistence of joint manifestations 52 Prognosis of extra-articular manifestations 56 5. Antibody response and presence of virus in tissues during human SINV infection (II, III, IV) 56 Antibody kinetics (III, IV) 56 Detection of SINV in blood and skin (II, III) 57 6. Epidemiology of SINV in Finland (II, V) 58 Molecular epidemiology of SINV strains from Finland (II) 58 Involvement of birds in the epidemiology of SINV (V) 59 SINV antibodies in resident grouse (Tetraonidae) in Finland (V) 61 SINV antibodies in migratory birds during spring migration (V) 62 Incidence and seroprevalence of SINV in human population in Finland (V) 63 CONCLUDING REMARKS AND PROSPECTS 66 ACKNOWLEDGMENTS 68 REFERENCES 70 ORIGINAL PUBLICATIONS I-V 83 SINDBIS VIRUS AND POGOSTA DISEASE IN FINLAND 5 – LIST OF ORIGINAL PUBLICATIONS – LIST OF ORIGINAL PUBLICATIONS The dissertation is based on the following original publications, which shall be referred to in the text by their Roman numerals (I-V). Some unpublished data are also presented. The copyright holders gave permission to reprint the articles. I Tytti MANNI, Satu KURKELA, Antti VAHERI, Olli VAPALAHTI Diagnostics of Pogosta disease: Antigenic properties and evaluation of Sindbis virus IgM and IgG enzyme immunoassays Vector-Borne and Zoonotic Diseases, in press II Satu KURKELA, Tytti MANNI, Antti VAHERI, Olli VAPALAHTI Causative agent of Pogosta disease isolated from blood and skin lesions Emerging Infectious Diseases 2004;10:889-894 III Satu KURKELA, Tytti MANNI, Johanna MYLLYNEN, AnttiVAHERI, Olli VAPALAHTI Clinical and laboratory manifestations of Sindbis virus infection: Prospective study, Finland, 2002-2003 The Journal of Infectious Diseases 2005;191:1820-1829 IV Satu KURKELA, Tapani HELVE, Antti VAHERI, Olli VAPALAHTI Arthritis and arthralgia three years after Sindbis virus infection: Clinical study of a cohort of 49 patients Scandinavian Journal of Infectious Diseases, in press V Satu KURKELA, Osmo RÄTTI, Eili HUHTAMO, Nathalie Yumari UZCÁTEGUI, Juha Pekka NUORTI, Juha LAAKKONEN, Tytti MANNI, Pekka HELLE, Antti VAHERI, Olli VAPALAHTI Sindbis virus infection in migratory birds, grouse, and humans, Finland Emerging Infectious Diseases, in press 6 SATU KURKELA - ABBREVIATIONS - ABBREVIATIONS arbovirus arthropod-borne virus BFV Barmah Forest virus BSA bovine serum albumin C capsid protein CHIKV Chikungunya virus cDNA complementary deoxyribonucleic acid CPE cytopathic effect CSF cerebrospinal fluid E1 envelope glycoprotein 1 E2 envelope glycoprotein 2 EDTA ethylene diamine tetra-acetic acid EEEV eastern equine encephalitis virus EIA enzyme immunoassay HI hemagglutination inhibition IFA immunofluorescence assay MAYV Mayaro virus MEM minimal essential medium NT neutralization test OD optical density ONNV O’nyong-nyong virus PBS phosphate-buffered saline PCR polymerase chain reaction RRV Ross River virus RT-PCR reverse transcriptase polymerase chain reaction SDS-PAGE sodium dodecyl sulfate polyacrylamide gel electrophoresis SINV Sindbis virus VEEV Venezuelan equine encephalitis virus WEEV western equine encephalitis virus SINDBIS VIRUS AND POGOSTA DISEASE IN FINLAND 7 – ABSTRACT – ABSTRACT Sindbis virus (SINV) (genus Alphavirus, family Togaviridae) is an enveloped virus with a genome of single-stranded, positive-polarity RNA of 11.7 kilobases. SINV is widespread in Eurasia, Africa, and Australia, but clinical infection only occurs in a few geographically restricted areas, mainly in Northern Europe. In Europe, antibodies to SINV were detected from patients with fever, rash, and arthritis for the first time in the early 1980s in Finland. It became evident that the causative agent of this syndrome, named Pogosta disease, was closely related to SINV. The disease is also found in Sweden (Ockelbo disease) and in Russia (Karelian fever). Since 1974, for unknown reason, the disease has occurred as large outbreaks every seven years in Finland. This study is to a large degree based on the material collected during the 2002 Pogosta disease outbreak in Finland. We first developed SINV IgM and IgG enzyme immunoassays (EIA), based on highly purified SINV, to be used in serodiagnostics. The EIAs correlated well with the hemagglutination inhibition (HI) test, and all individuals showed neutralizing antibodies. The sensitivities of the IgM and IgG EIAs were 97.6% and 100%, and specificities 95.2% and 97.6%, respectively. E1 and E2 envelope glycoproteins of SINV were shown to be recognized by IgM and IgG in the immunoblot early in infection. We isolated SINV from five patients with acute Pogosta disease; one virus strain was recovered from whole blood, and four other strains from skin lesions. The etiology of Pogosta disease was confirmed by these first Finnish SINV strains, also representing the first human SINV isolates from Europe. Phylogenetic analysis indicated that the Finnish SINV strains clustered with the strains previously isolated from mosquitoes in Sweden and Russia, and seemed to have a common ancestor with South-African strains. Northern European SINV strains could be maintained locally in disease-endemic regions, but the phylogenetic analysis also 8 SATU KURKELA – ABSTRACT – suggests that redistribution of SINV tends to occur in a longitudinal direction, possibly with migratory birds. We searched for SINV antibodies in resident grouse (N=621), whose population crashes have previously coincided with human SINV outbreaks, and in migratory birds (N=836). SINV HI antibodies were found for the first time in birds during their spring migration to Northern Europe, from three individuals: red-backed shrike, robin, and song thrush. Of the grouse, 27.4% were seropositive in 2003, one year after a human outbreak, but only 1.4% of the grouse were seropositive in 2004. Thus, grouse might contribute to the human epidemiology of SINV. A total of 86 patients with verified SINV infection
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