Diversité génétique d’Anaplasma Phagocytophilum, agent de l’anaplasmose granulocytaire, conséquences épidemiologiques et implications pour le contrôle en France

Anaplasma phagocytophilum is a tick-borne bacterium and the etiologic agent of granulocytic anaplasmosis, an emerging disease that affects a wide range of mammals. In this paper, we present the recent knowledge gained from studies on the genetic diversity of this pathogen in France. Multilocus sequence analysis (MLSA) was used to characterize the genetic diversity of A. phagocytophilum in populations of French cattle, horses, dogs, and roe deer. MLSA was based on nine loci (ankA, msp4, groESL, typA, pled, gyrA, recG, polA, and an intergenic region). Phylogenic analysis revealed three genetic clusters of bacterial variants in domesticated animals. The two principal clusters included 98% of the bacterial genotypes found in cattle, which were only distantly related to those in roe deer. One cluster comprised only cattle genotypes, while the second contained genotypes from cattle, horses, and dogs. The third contained all roe deer genotypes and three cattle genotypes. These results suggest that roe deer do not contribute to the spread of A. phagocytophilum in cattle in France. A Multiple-Locus Variable number tandem repeat (VNTR) Analysis typing technique was developed for A. phagocytophilum. Five VNTRs were selected based on the HZ human-derived strain genome, and were tested on the Webster human-derived strain and on 123 DNA samples. This study confirmed that A. phagocytophilum from roe deer or domestic ruminants belong to two different clusters, while A. phagocytophilum from red deer and domestic ruminants locate within the same cluster, questioning the respective roles of roe vs red deer as reservoir hosts for domestic ruminant strains in Europe. The molecular techniques recently developed have great potential to provide detailed information on A. phagocytophilum isolates,improving both epidemiological and phylogenic investigations, thereby helping in the development of relevant prevention and control measures.

[1]  V. Loux,et al.  Comparative genomics of first available bovine Anaplasma phagocytophilum genome obtained with targeted sequence capture , 2014, BMC Genomics.

[2]  F. Corbière,et al.  A new multiple-locus variable-number tandem repeat analysis reveals different clusters for Anaplasma phagocytophilum circulating in domestic and wild ruminants , 2014, Parasites & Vectors.

[3]  M. Ganter,et al.  Analysis of the Population Structure of Anaplasma phagocytophilum Using Multilocus Sequence Typing , 2014, PloS one.

[4]  R. Birtles,et al.  Anaplasma phagocytophilum strains from voles and shrews exhibit specific ankA gene sequences , 2013, BMC Veterinary Research.

[5]  J. de la Fuente,et al.  Subolesin/Akirin vaccines for the control of arthropod vectors and vectorborne pathogens. , 2013, Transboundary and emerging diseases.

[6]  E. G. Granquist,et al.  Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies , 2013, Front. Cell. Infect. Microbiol..

[7]  X. Bailly,et al.  Single Genotype of Anaplasma phagocytophilum Identified from Ticks, Camargue, France , 2013, Emerging infectious diseases.

[8]  William H. Offenhauser,et al.  Wild Boars as Hosts of Human-Pathogenic Anaplasma phagocytophilum Variants , 2012, Emerging infectious diseases.

[9]  J. Foley,et al.  Antigen variability in Anaplasma phagocytophilum during chronic infection of a reservoir host. , 2012, Microbiology.

[10]  C. Gortázar,et al.  Gene expression profile suggests that pigs (Sus scrofa) are susceptible to Anaplasma phagocytophilum but control infection , 2012, Parasites & Vectors.

[11]  B. Durand,et al.  Population Structure of Bartonella henselae in Algerian Urban Stray Cats , 2012, PloS one.

[12]  A. Radford,et al.  Recurrent bacteraemia in sheep infected persistently with Anaplasma phagocytophilum. , 2012, Journal of comparative pathology.

[13]  J. de la Fuente,et al.  Sheep experimentally infected with a human isolate of Anaplasma phagocytophilum serve as a host for infection of Ixodes scapularis ticks. , 2012, Ticks and tick-borne diseases.

[14]  Qiang Chen,et al.  Expression and Immunogenicity of Recombinant Immunoreactive Surface Protein 2 of Anaplasma phagocytophilum , 2012, Clinical and Vaccine Immunology.

[15]  H. Taraschewski,et al.  The European hedgehog (Erinaceus europaeus)--a suitable reservoir for variants of Anaplasma phagocytophilum? , 2012, Ticks and tick-borne diseases.

[16]  D. Meyer,et al.  A new typing technique for the Rickettsiales Ehrlichia ruminantium: multiple-locus variable number tandem repeat analysis. , 2012, Journal of microbiological methods.

[17]  R. Birtles,et al.  The common shrew (Sorex araneus): a neglected host of tick-borne infections? , 2011, Vector borne and zoonotic diseases.

[18]  Y. Rikihisa.  Mechanisms of Obligatory Intracellular Infection with Anaplasma phagocytophilum , 2011, Clinical Microbiology Reviews.

[19]  H. Steinshamn,et al.  A comparative study of clinical manifestations, haematological and serological responses after experimental infection with Anaplasma phagocytophilum in two Norwegian sheep breeds , 2011, Acta veterinaria Scandinavica.

[20]  J. Dumler,et al.  Distinct Host Species Correlate with Anaplasma phagocytophilum ankA Gene Clusters , 2010, Journal of Clinical Microbiology.

[21]  Y. Rikihisa,et al.  Microreview: Type IV secretion in the obligatory intracellular bacterium Anaplasma phagocytophilum , 2010, Cellular microbiology.

[22]  H. Sultana,et al.  Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. , 2010, The Journal of clinical investigation.

[23]  K. Bergström,et al.  EXPERIMENTAL INFECTION IN LAMBS WITH A RED DEER (CERVUS ELAPHUS) ISOLATE OF ANAPLASMA PHAGOCYTOPHILUM , 2010, Journal of wildlife diseases.

[24]  K. Bergström,et al.  Variant -and individual dependent nature of persistent Anaplasma phagocytophilum infection , 2010, Acta veterinaria Scandinavica.

[25]  Y. Rikihisa.  Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells , 2010, Nature Reviews Microbiology.

[26]  Z. Woldehiwet.  The natural history of Anaplasma phagocytophilum. , 2010, Veterinary parasitology.

[27]  M. Begon,et al.  Delineating Anaplasma phagocytophilum Ecotypes in Coexisting, Discrete Enzootic Cycles , 2009, Emerging infectious diseases.

[28]  B. Chomel,et al.  Comparison of the performances of MLVA vs. the main other typing techniques for Bartonella henselae. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[29]  J. Foley,et al.  Canine granulocytic anaplasmosis: a review. , 2009, Journal of veterinary internal medicine.

[30]  S. Caracappa,et al.  Prevalence and Genotypes of Anaplasma Species and Habitat Suitability for Ticks in a Mediterranean Ecosystem , 2008, Applied and Environmental Microbiology.

[31]  A. Rymaszewska.  Divergence within the marker region of the groESL operon in Anaplasma phagocytophilum , 2008, European Journal of Clinical Microbiology & Infectious Diseases.

[32]  R. Birtles,et al.  Dynamic Transmission of Numerous Anaplasma phagocytophilum Genotypes among Lambs in an Infected Sheep Flock in an Area of Anaplasmosis Endemicity , 2008, Journal of Clinical Microbiology.

[33]  Z. Woldehiwet.  Immune evasion and immunosuppression by Anaplasma phagocytophilum, the causative agent of tick-borne fever of ruminants and human granulocytic anaplasmosis. , 2008, Veterinary journal.

[34]  Y. Rikihisa,et al.  Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl‐1 to facilitate infection † , 2007, Cellular microbiology.

[35]  A. Lundgren,et al.  Outer Membrane Protein Sequence Variation in Lambs Experimentally Infected with Anaplasma phagocytophilum , 2007, Infection and Immunity.

[36]  S. Stuen.  Anaplasma Phagocytophilum - the Most Widespread Tick-Borne Infection in Animals in Europe , 2007, Veterinary Research Communications.

[37]  S. Shukla,et al.  Contribution of Polymorphisms in ankA, gltA, and groESL in Defining Genetic Variants of Anaplasma phagocytophilum , 2007, Journal of Clinical Microbiology.

[38]  R. Birtles,et al.  High-Resolution Genetic Fingerprinting of European Strains of Anaplasma phagocytophilum by Use of Multilocus Variable-Number Tandem-Repeat Analysis , 2007, Journal of Clinical Microbiology.

[39]  B. Durand,et al.  Development of discriminatory multiple-locus variable number tandem repeat analysis for Bartonella henselae. , 2007, Microbiology.

[40]  M. Begon,et al.  Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? , 2006, Vector borne and zoonotic diseases.

[41]  J. Sattabongkot,et al.  Genetic structures of geographically distinct Plasmodium vivax populations assessed by PCR/RFLP analysis of the merozoite surface protein 3beta gene. , 2006, Acta tropica.

[42]  Manoj N. Krishnan,et al.  An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands , 2006, The Journal of experimental medicine.

[43]  J. André,et al.  VACCINATION, WITHIN-HOST DYNAMICS, AND VIRULENCE EVOLUTION , 2006 .

[44]  N. Ogden,et al.  Detection by the polymerase chain reaction of Anaplasma phagocytophilum in tissues of persistently infected sheep. , 2006, Journal of comparative pathology.

[45]  M. F. Addis,et al.  Equine and Canine Anaplasma phagocytophilum Strains Isolated on the Island of Sardinia (Italy) Are Phylogenetically Related to Pathogenic Strains from the United States , 2005, Applied and Environmental Microbiology.

[46]  Bjørn‐Arne Lindstedt,et al.  Multiple‐locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria , 2005, Electrophoresis.

[47]  J. Foley,et al.  Differences in the Transmissibility of Two Anaplasma phagocytophilum Strains by the North American Tick Vector Species, Ixodes Pacificus and Ixodes Scapularis (Acari: Ixodidae) , 2005, Experimental & Applied Acarology.

[48]  T. Mather,et al.  Inability of a variant strain of Anaplasma phagocytophilum to infect mice. , 2003, The Journal of infectious diseases.

[49]  C. Bogdan,et al.  High Diversity of ankA Sequences of Anaplasma phagocytophilum among Ixodes ricinus Ticks in Germany , 2003, Journal of Clinical Microbiology.

[50]  T. Moum,et al.  Fatal Cases of Tick‐Borne Fever (TBF) in Sheep Caused by Several 16S rRNA Gene Variants of Anaplasma phagocytophilum , 2003, Annals of the New York Academy of Sciences.

[51]  N. Ogden,et al.  Transmission of Anaplasma phagocytophilum to Ixodes ricinus Ticks from Sheep in the Acute and Post-Acute Phases of Infection , 2003, Infection and Immunity.

[52]  K. Bown,et al.  Natural Ehrlichia phagocytophila transmission coefficients from sheep ‘carriers’ to Ixodes ricinus ticks vary with the numbers of feeding ticks , 2002, Parasitology.

[53]  N. Ogden,et al.  Field evidence for density-dependent facilitation amongst Ixodes ricinus ticks feeding on sheep , 2002, Parasitology.

[54]  S. Ray,et al.  Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and , 2001, International journal of systematic and evolutionary microbiology.

[55]  S. Malawista,et al.  Exploitation of Interleukin-8-Induced Neutrophil Chemotaxis by the Agent of Human Granulocytic Ehrlichiosis , 2001, Infection and Immunity.

[56]  Philippe Brouqui,et al.  Analysis of the 16S rRNA Gene Sequence of Anaplasma centrale and Its Phylogenetic Relatedness to Other Ehrlichiae , 2001, Clinical Diagnostic Laboratory Immunology.

[57]  Y. Rikihisa,et al.  Intracellular Infection by the Human Granulocytic Ehrlichiosis Agent Inhibits Human Neutrophil Apoptosis , 2000, Infection and Immunity.

[58]  J. Dawson,et al.  Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Bakken,et al.  Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease , 1994, Journal of clinical microbiology.

[60]  Z. Woldehiwet,et al.  Stages in the development of Cytoecetes phagocytophila, the causative agent of tick-borne fever. , 1982, Journal of comparative pathology.

[61]  B. Madewell,et al.  Infection in two dogs with an agent resembling Ehrlichia equi. , 1982, Journal of the American Veterinary Medical Association.

[62]  A. Foggie.  Studies on the infectious agent of tick-borne fever in sheep. , 1951, The Journal of pathology and bacteriology.

[63]  J. Macleod,et al.  Studies in Tick-borne Fever of Sheep. I. Transmission by the Tick, Ixodes ricinus, with a Description of the Disease Produced , 1933, Parasitology.