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Pär Comstedt UMEÅ UNIVERSITY MEDICAL DISSERTATIONS New Series No. 1161 ISSN 0346-6612 ISBN 978-91-7264-521-9 Editor: The Dean of the Faculty of Medicine Biology of Borrelia garinii Spirochetes Pär Comstedt Department of Molecular Biology Laboratory for Molecular Infection Medicine Sweden (MIMS) Umeå University, Sweden 2008 To Erik Bengtsson Copyright © Pär Comstedt Printed by Print & Media 2008 Design: Anna Bolin Table of contents ABSTRACT.................................................................................................................1 Papers in this thesis.....................................................................................................2 Papers not included in this thesis...............................................................................3 Abbreviations and terms ............................................................................................4 INTRODUCTION.........................................................................5 The history of Lyme borreliosis .................................................................................5 Zoonoses.......................................................................................................................6 Vector-borne diseases .................................................................................................7 Birds as reservoirs for zoonoses.................................................................................8 Classification................................................................................................................9 The Lyme Borrelia genospecies..............................................................................11 General characteristics ............................................................................................11 Geographical distribution.........................................................................................12 Clinical manifestations of Lyme borreliosis............................................................13 Diagnosis and treatment ...........................................................................................14 Prevention..................................................................................................................14 High risk areas.........................................................................................................14 The Lyme borreliosis vaccine .................................................................................15 Genetic manipulation................................................................................................16 In vitro cultivation .....................................................................................................17 Typing........................................................................................................................17 Phenotypic ..............................................................................................................17 Genotypic................................................................................................................18 The infection cycle ....................................................................................................18 The tick vector...........................................................................................................19 Ixodes ricinus complex ...........................................................................................19 Ixodes uriae ............................................................................................................21 Transfer of infection from the tick to the host .......................................................22 Spirochete protein expression in the tick and the skin ..........................................23 Reservoir hosts..........................................................................................................24 Reservoir hosts in North America...........................................................................24 Reservoir hosts in Europe.......................................................................................25 Poor reservoir hosts ................................................................................................26 The complicated biology of B. garinii....................................................................27 Borrelia and birds .....................................................................................................28 Experimental infections of birds.............................................................................28 Borrelia spirochetes and terrestrial birds................................................................29 The impact of bird migration ..................................................................................30 B. garinii and seabirds ............................................................................................31 Interaction between the marine and the terrestrial infection cycles ........................32 The complement system ...........................................................................................33 Regulation of the alternative pathway ....................................................................34 Complement evasion...............................................................................................34 Differences among Lyme Borrelia spirochetes ......................................................35 AIMS OF THE THESIS............................................................. 37 RESULTS AND DISCUSSION................................................. 39 Paper I. ......................................................................................................................39 Birds as carriers of ticks..........................................................................................39 Passerine birds as hosts for B. garinii infected ticks...............................................40 Reservoir competence of passerine birds ................................................................40 Clinical importance of Lyme Borrelia spirochetes spread by birds ........................41 Paper II. .....................................................................................................................43 Presence of Borrelia spirochetes in the Arctic........................................................43 Similarities to other Borrelia isolates......................................................................43 Paper III.....................................................................................................................45 Prevalence and densities of spirochetes among ticks and seabirds .........................45 Genetic polymorphism ............................................................................................46 Phylogeny................................................................................................................46 Paper IV.....................................................................................................................49 The marine and the terrestrial infection cycle .........................................................49 Complement resistance properties...........................................................................49 Paper V.......................................................................................................................51 OspE expression and complement resistance..........................................................51 Factor H binding proteins of B. garinii ...................................................................51 CONCLUSIONS........................................................................53 SAMMANFATTNING ................................................................55 Acknowledgements....................................................................................................57 References..................................................................................................................58 ABSTRACT Lyme borreliosis is a tick-transmitted infectious disease. The causative agents are spiral-shaped bacteria and the most common sign of infection is a skin rash at the site of the tick bite. If not treated with antibiotics, the bacteria can disseminate and cause a variety of different manifestations including arthritis, carditis or neurological problems. The disease is a zoonosis and the bacteria are maintained in nature by different vertebrate reservoir host animals. In Europe, three different Borrelia genospecies cause Lyme borreliosis: B. burgdorferi, B. afzelii and B. garinii. The latter depends in part on birds as its reservoir host. B. garinii bacteria have been found in a marine enzootic infection cycle worldwide and also among terrestrial birds. This thesis suggests that passerine birds and seabirds constitute an important reservoir for B. garinii bacteria also with clinical importance. We have found bacteria very similar to Lyme borreliosis causing isolates in ticks infesting migrating passerine birds. The birds not only transport infected ticks, but are competent reservoir hosts, as measured by their ability to infect naïve ticks. Their role as a reservoir host is dependent on their foraging behavior, where ground-dwelling birds are of greater importance than other species. When comparing B. garinii isolates from Europe, the Arctic and North Pacific, and including isolates from seabirds, passerine birds,
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