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Anaplasma Phagocytophilum and Human Granulocytic Anaplasmosis in Portugal

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Anaplasma Phagocytophilum and Human Granulocytic Anaplasmosis in Portugal UNIVERSIDADE NOVA DE LISBOA INSTITUTO DE HIGIENE E MEDICINA TROPICAL Anaplasma phagocytophilum and human granulocytic anaplasmosis in Portugal Ana Sofia Pereira dos Santos Dissertação apresentada ao Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, para obtenção do Grau de Doutor no Ramo de Ciências Biomédicas, Especialidade de Microbiologia LISBOA 2007 Neutrophil with Anaplasma phagocytophilum morulae. Pheripheral blood smear stained with Diff-Quik. Photograph kindly provided by Professor J Stephen Dumler, The Johns Hopkins University School of Medicine, Baltimore. Neutrófilo com uma mórula de Anaplasma phagocytophilum. Esfregaço de sangue periférico corado com Diff-Quik. Fotografia gentilmente cedida pelo Professor J Stephen Dumler, The Johns Hopkins University School of Medicine, Baltimore. Este trabalho foi financiado pela Fundação para a Ciência e a Tecnologia através da atribuição da bolsa de doutoramento refª SFRH/BD/8610/2002. ORIENTAÇÃO: Doutora Fátima Bacellar Investigadora Principal Aposentada Centro de Estudos de Vectores e Doenças Infecciosas Instituto Nacional de Saúde Dr. Ricardo Jorge, Lisboa Professor John Stephen Dumler Professor Associado Division of Medical Microbiology, Department of Pathology The Johns Hopkins University School of Medicine, Baltimore COMISSÃO TUTORIAL: Doutora Margarida Collares Pereira Investigadora Principal com Habilitação Instituto de Higiene e Medicina Tropical Universidade Nova de Lisboa, Lisboa Professor Doutor Paulo Almeida Professor Associado Instituto de Higiene e Medicina Tropical Universidade Nova de Lisboa, Lisboa Doutora Fátima Bacellar Investigadora Principal Aposentada Centro de Estudos de Vectores e Doenças Infecciosas Instituto Nacional de Saúde Dr. Ricardo Jorge, Lisboa Na presente dissertação incluem-se resultados que foram ou estão a ser alvo de publicação em co-autoria. Para efeitos do disposto no nº1 do Despacho nº2303/2000 do Regulamento de Programas de Doutoramento do Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa (Diário da República, 2ª série, nº23, de 28 de Janeiro de 2000), o autor da dissertação declara que interveio na concepção e execução do trabalho experimental, na interpretação dos resultados e na redacção dos manuscritos publicados, no prelo ou que aguardam submissão. Lisboa, 11 de Setembro de 2007 Ana Sofia Pereira dos Santos a Arminda ACKNOWLEGEMENTS / AGRADECIMENTOS Ao Instituto Nacional de Saúde Dr. Ricardo Jorge (INSA) a possibilidade de realizar os trabalhos que permitiram a elaboração da presente dissertação; À Fundação para a Ciência e a Tecnologia, a atribuição da bolsa de doutoramento (refª SFRH/BD/8610/2002), sem a qual teria sido impossível a realização deste projecto; Ao Professor Doutor Armindo Filipe e Doutora Maria Sofia Núncio, responsáveis pelo Centro de Estudos de Vectores e Doenças Infecciosas, Instituto Nacional de Saúde Dr. Ricardo Jorge (CEVDI/INSA), em diferentes fases do meu percurso, pelo apoio e incentivo que tenho merecido desde os primeiros passos no mundo da Ciência e pela disponibilização de todos os recursos do Centro para o bom andamento da parte experimental desta dissertação; À Doutora Fátima Bacellar, minha orientadora no CEVDI/INSA e mentora, a quem devo a minha formação, o apoio incondicional e a amizade que tem sido uma constante desde que as nossas vidas se cruzaram; To Professor John Stephen Dumler, my sponsor at The Johns Hoopkins University School of Medicine, for all the knowledge, support and stimulation. I am grateful for knowing you and honoured to be able to share some of your expertise in A. phagocytophilum field. À Doutora Margarida Collares Pereira e ao Professor Doutor Paulo Almeida, por terem aceite ser o elo de ligação ao Instituto de Higiene e Medicina Tropical (IHMT), e que com as suas sugestões, apoio e incentivo simplificaram várias etapas deste trabalho; Ao Professor Doutor Virgílio do Rosário e Professora Doutora Maria Amélia Grácio, anterior e actual Presidente do Conselho Científico do IHMT, pelo acolhimento institucional e disponibilidade na resolução de todas as questões académicas determinantes para a boa consecução deste projecto; Ao Mestre João Lavinha, ex-Director do INSA e presentemente responsável pelo Centro de Genética Humana do mesmo Instituto, por acreditar e apoiar todos os projectos que me proponho desenvolver; To all the Researchers that since a long time have collaborated with CEVDI/INSA in Anaplasmatacea field, from which the work developed in this dissertation has beneficiated, especially to Jackie Dawson from CDC - Atlanta, Professor Didier Raoult and Philipe Brouqui from Unité des Rickettsie - Marseille, José António Oteo and Arantza Portillo from Hospitales San Millán-San Pedro de La Rioja – Logroño. Também aos Investigadores portugueses, Professor Doutor João David de Morais, Doutora Susana da Franca, Professor Doutor Victor Caeiro e Professor Doutor António José do Santos Grácio, com quem tive o privilégio de colaborar em várias etapas do meu percurso científico. A presente dissertação é ainda testemunho da cooperação, dedicação e amizade de muitos a quem gostaria de expressar o meu profundo reconhecimento, como os colegas e amigos do CEVDI/INSA, do Dumler’s lab, do Laboratório de Microbiologia e Ecologia e da Unidade de leptospirose e borreliose de Lyme; Por último, aos primeiros em matéria de partilha de sofrimento e alegrias nestas etapas da minha vida, aos meus pais, em nome de toda a família, amigos e ao Jorge. Foi por vós que aqui cheguei… Abstract / Resumo ABSTRACT Anaplasma phagocytophilum and granulocytic anaplasmosis are of increasing interest to the scientific community as indicated by the expanding number of reports published in the past two decades, and especially since the emergence of the first cases of human granulocytic anaplasmosis (HGA). The growing recognition of the Public Health importance of A. phagocytophilum in North America and in Europe, along with its recent detection in Portugal has signalled the need for more detailed studies that address the emergence of HGA and its causative agent in our country. Initially based on an methodological training in research units dedicated to Anaplasmataceae, this work enabled the transfer of technology as currently applied to A. phagocytophilum research and made possible the development of a new line of investigation at Centro de Estudos de Vectores e Doenças Infecciosas, Instituto Nacional de Saúde Dr. Ricardo Jorge (CEVDI/INSA). By establishing the foundations for concerted study on A. phagocytophilum and HGA, the work described herein has facilitated development of a broad approach toward fundamental issues in Anaplasmataceae ecobiology and disease by focusing attention on identification of potential ixodid vectors, mammals likely to be involved in the infectious agent’s life cycles either as reservoirs or affected hosts, and garnered the evidence indicating the potential for human exposure in Portugal. The studies conducted in ixodid ticks proves the involvement of two Ixodes species in A. phagocytophilum cycles, including Ixodes ricinus on Madeira Island and I. ventalloi on the mainland. The detection of A. phagocytophilum DNA in I. ricinus reinforces prior studies and suggests its persistence on Madeira Island. This thesis also adds new data to the understanding of the natural history of A. phagocytophilum by providing the first evidence of infections in I. ventalloi ticks. The fact that some infected arthropods infest domestic cats not only mandates the inclusion of these mammals on the national list of vertebrate hosts parasitized by I. ventalloi ticks, but also shows their potential complicity in A. phagocytophilum maintenance. Moreover, molecular data shows the existence of A. phagocytophilum variant genotypes in Portuguese ticks. Partial gene sequences from infected ticks demonstrates nucleotide polymorphisms that support a close relationship of A. phagocytophilum on Madeira Island I. ricinus to North American strains isolated from humans as well as genotypes detected in Central and Northern Europe. Yet, these variants diverge from those found in mainland I. ventalloi, which represents a new genotype of undetermined pathogenicity. Serological evidence of exposure to A. phagocytophilum or a close related agent is shown in Mus spretus mice, horses, and dogs in mainland. Molecular analysis of biological samples from these animal populations provides the first definitive evidence of A. phagocytophilum active infection in Portuguese vertebrates with detection of its DNA in one seropositive horse from mainland Portugal, where the A. xi phagocytophilum genotype found is closely related to strains isolated from humans, suggesting the potential for HGA in Portugal. This thesis further extends study to identification of another closely related Anaplasma species, and its potential for serological cross-reactions with A. phagocytophilum, as evident with the detection of A. platys DNA in seropositive dogs. These data also underscore the importance of veterinarians maintaining vigilance for detection of not only granulocytic anaplasmosis but also canine infectious cyclic thrombocytopenia as causes of tick-borne diseases in Portugal. Both prospective and retrospective serological and molecular investigations of human exposure to A. phagocytophilum were performed on samples received at CEVDI/INSA for the laboratory diagnosis of patients with suspected tick-borne diseases during 2000-2006. The results provide evidence for seropositive Portuguese patients, including
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