High prevalence of Borrelia burgdorferi s.l. in the European red squirrel Sciurus vulgaris in France

Ticks and Tick-borne Diseases

Volumn 5, Issue 1, 2014, Pages 1-6

  Pisanu, Benoît ^a   Chapuis, Jean Louis ^a   Dozières, Anne ^a   Basset, Franck ^b   Poux, Valérie ^c   Vourc'h, Gwenaël ^c  

^a CNRS   (France)

^b Office National des Forêts ^*  (France)

^c EPIA   (France)

Author keywords

Biogeography; Borrelia burgdorferi s.s.; European red squirrel; Ixodes ricinus; Sciurus vulgaris

Indexed keywords

ARTICLE; BACTERIUM DETECTION; BIOGEOGRAPHIC REGION; BODY MASS; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA BURGDORFERI SENSU LATO; BORRELIA GARINII; CONTROLLED STUDY; FRANCE; HOST PATHOGEN INTERACTION; IXODES RICINUS; IXODES TRIANGULICEPS; LARVA; LYME DISEASE; MALE; NONHUMAN; NYMPH; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PREVALENCE; PRIORITY JOURNAL; SCIURUS; SCIURUS VULGARIS; SEASONAL VARIATION; SPECIES DIVERSITY; SPECIES IDENTIFICATION; TICK; ANIMAL; CHEMISTRY; DISEASE CARRIER; FEMALE; GENETICS; GEOGRAPHY; HUMAN; ISOLATION AND PURIFICATION; IXODES; MICROBIOLOGY; PARASITE VECTOR; PARASITOLOGY; SCIURIDAE;

BORRELIA BURGDORFERI; IXODES RICINUS; IXODIDA; IXODIDAE; RODENTIA; SCIURIDAE; SCIURUS VULGARIS; TAMIASCIURUS;

BACTERIAL DNA;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI GROUP; DISEASE RESERVOIRS; DNA, BACTERIAL; FEMALE; FRANCE; GEOGRAPHY; HUMANS; IXODES; LARVA; LYME DISEASE; MALE; NYMPH; PREVALENCE; SCIURIDAE;

EID: 84888323317     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2013.07.007     Document Type: Article

References (57)

1. Baranton G., De Martino S.J. Borrelia burgdorferi sensu lato diversity and its influence on pathogenicity in humans. Lyme Borreliosis: Biological and Clinical Aspects 2009, 1-17. Karger, Basel, Switzerland. D. Lipsker, B. Jaulhac (Eds.).
2. Barton K. MuMIn: Multi-Model Inference 2012, http://www.r-forge.r-project.org/projects/mumin/.
3. Bjornstad O.N. ncf: Spatial Nonparametric Covariance Functions. R package Version 1.1-3 2009, http://www.cran.r-project.org/package=ncf.
4. Brisson D., Dykhuizen D.E., Ostfeld R.S. Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proc. R. Soc. Lond. B 2008, 275:227-235.
5. Chapuis J.-L., Obolenskaya E.V., Pisanu B., Lissovsky A.A. Tamias sibiricus (Siberian chipmunk) Datasheet. Invasive Species 2011, Cambridge Agricultural Bureau International, Available from: http://www.cabi.org/isc (last modified 05.01.12).
6. Craine N.G., Nuttall P.A., Mariott A.C., Randolph S.E. Role of grey squirrels and pheasants in the transmission of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete, in the U.K. Folia Parasitol. 1997, 44:155-160.
7. Derdáková M., Dudiòák V., Brei B., Brownstein J.S., Schwartz I., Fish D. Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Appl. Environ. Microbiol. 2004, 70:6783-6788.
8. Derdáková M., Lenčáková D. Association of genetic variability within the Borrelia burgdorferi sensu lato with the ecology, epidemiology of Lyme borreliosis in Europe. Ann. Agric. Environ. Med. 2005, 12:165-172.
9. Estrada-Peña A., Ortega C., Sánchez N., DeSimone L., Sudre B., Suk J.E., Semanza J.C. Correlation of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks with specific abiotic traits in the Western Palearctic. App. Environ. Microbiol. 2011, 77:3838-3845.
10. Franke J., Moldenhauer A., Hildebrandt A., Dorn W. Are birds reservoir hosts for Borrelia afzelii?. Ticks Tick-Borne Dis. 2010, 1:109-112.
11. Gern L. Life cycle of Borrelia burgdorferi sensu lato and transmission to humans. Lyme Borreliosis: Biological and Clinical Aspects 2009, 18-30. Karger, Basel, Switzerland. D. Lipsker, B. Jaulhac (Eds.).
12. Gern L., Douet V., López Z., Rais O., Morán Cadenas F. Diversity of Borrelia genospecies in Ixodes ricinus ticks in a Lyme borreliosis endemic area in Switzerland identified by using new probes for reverse line blotting. Ticks Tick-Borne Dis. 2010, 1:23-29.
13. Gern L., Humair P.-F. Ecology of Borrelia burgdorferi sensu lato in Europe. Lyme Borreliosis: Biology, Epidemiology and Control 2002, 149-174. C.A.B. International, UK. J.S. Gray, O. Kahl, R.S. Lane, G. Stanek (Eds.).
14. Gilot B., Pérez-Eid C. Bio-écologie des tiques induisant les pathologies les plus importantes en France. Méd. Mal. Infect. 1998, 28:325-334.
15. Gurnell J. The Natural History of Squirrels 1987, Christopher Helm mammal series, London, Oxford, U.K.
16. Hanincová K., Kurtenbach K., Diuk-Wasser M., Brei B., Fish D. Epidemic spread of Lyme borreliosis, northeastern United States. Emerg. Infect. Dis. 2006, 12:604-611.
17. Hanincová K., Schäffer S.M., Etti S., Sewell H.-S., Taragelová V., Ziak D., Labuda M., Kurtenbach K. Association of Borrelia afzelii with rodents in Europe. Parasitology 2003, 126:11-20.
18. Huegli D., Hu C.M., Humair P.-F., Wilske B., Gern L. Apodemus species mice, reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J. Clin. Microbiol. 2002, 40:4735-4737.
19. Humair P.-F., Gern L. Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Trop. 1998, 69:213-227.
20. Humair P.-F., Gern L. The wild hidden face of Lyme borreliosis in Europe. Microbes Infect. 2000, 2:915-922.
21. Humair P.-F., Rais O., Gern L. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 1999, 118:33-42.
22. Inventaire national du Patrimoine naturel Cartes et information géographique 2012, INPN, http://www.inpn.mnhn.fr/telechargement/cartes-et-information-geographique [8 février 2012]. Muséum national d'Histoire naturelle (Ed.).
23. Kurtenbach K., Dizij A., Seitz H.M., Margos G., Moter S.E., Kramer M.D., Wallich R., Schaible U.E., Simon M.M. Differential immune response to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L. (Acari Ixodidae). Infect. Immun. 1994, 62:5344-5352.
24. Kurtenbach K., Hanincova K., Tsao J.I., Margos G., Fish D., Ogden N.H. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 2006, 4:660-669.
25. Kurtenbach K., Peacey M., Rijpkema S.G.T., Hoodless A.N., Nuttall P.A., Randolph S.E. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl. Environ. Microbiol. 1998, 64:1169-1174.
26. Lane R.S., Mun J., Eisen R.J., Eisen L. Western gray squirrel (Rodentia: Sciuridae): a primary reservoir host of Borrelia burgdorferi in Californian oak woodlands?. J. Med. Entomol. 2005, 42:388-396.
27. LoGiudice K., Ostfeld R.S., Schmidt K.A., Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:567-571.
28. Lurz P.W.W., Gurnell J., Magris L. Sciurus vulgaris. Mammalian Species 2005, 769:1-10.
29. Margos G., Gatewood A.G., Aanensen D.M., Hanincová K., Terekhova D., Vollmer S.A., Cornet M., Piesman J., Donaghy M., Bormane A., Hurn M.A., Feil E.J., Fish D., Casjens S., Wormser G.P., Schwartz I., Kurtenbach K. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8730-8735.
30. Margos G., Vollmer S.A., Cornet M., Garnier M., Fingerle V., Wilske B., Bormane A., Vitorino L., Collares-Pereira M., Drancourt M., Kurtenbach K. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl. Environ. Microbiol. 2009, 75:5410-5416.
31. Marsot M., Sigaud M., Chapuis J.-L., Ferquel E., Cornet M., Vourc'h G. Introduced Siberian chipmunks (Tamias sibiricus) harbor more diverse Borrelia burgdorferi sensu lato genospecies than native bank voles (Myodes glareolus). Appl. Environ. Microbiol. 2011, 77:5716-5721.
32. Marsot M., Chapuis J.-L., Gasqui P., Dozières A., Masséglia S., Pisanu B., Ferquel E., Vourc'h G. Introduced Siberian chipmunks (Tamias sibiricus barberi) contribute more to Lyme borreliosis risk than native reservoir rodents. PLoS ONE 2013, 8:e55377.
33. Mather T.N., Wilson M.L., Moore S.I., Ribeiro J.M., Spielman A. Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). Am. J. Epidemiol. 1989, 130:143-150.
34. Medlock J.M., Hansford K.M., Bormane A., Derdáková M., Estrada-Peña A., George J.-C., Golovljova I., Jaenson T.G.T., Jensen J.-K., Jensen P.M., Kazimirova K., Oteo J.A., Papa A., Pfister K., Plantard O., Randolph S.E., Rizzoli A., Santos-Silva M.M., Sprong H., Vial L., Hendrickx G., Zeller H., Van Bortel W. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasite Vector 2013, 6:1.
35. Michalik J., Skotarczak B., Skoracki M., Wodecka B., Sikora B., Hofman T., Rymaszewska A., Sawczuk M. Borrelia burgdorferi sensu stricto in yellow-necked mice and feeding Ixodes ricinus ticks in a forest habitat of West central Poland. J. Med. Entomol. 2005, 42:850-856.
36. Nieto N.C., Leonhard S., Foley J.E., Lane R.S. Coinfection of Western gray squirrel (Sciurus griseus) and other sciurid rodents with Borrelia burgdorferi sensu stricto and Anaplasma phagocytophilum in California. J. Wildl. Dis. 2010, 46:291-296.
37. Pérez-Eid C. Les tiques: identification, biologie, importance médicale et vétérinaire 2007, Lavoisier, Paris, France.
38. Piesman J., Gern L. Lyme borreliosis in Europe and North America. Parasitology 2004, 129:S191-S220.
39. Pisanu B., Obolenskaya E.V., Baudry E., Lissovsky A.A., Chapuis J.-L. Narrow phylogeographical origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia, Sciuridae) established in France. Biol. Invasions 2013, 15:1201-1207.
40. Poupon M.-A., Lommano E., Humair P.F., Douet V., Rais O., Schaad M., Jenni L., Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl. Environ. Microbiol. 2006, 72:976-979.
41. R Core Team R: A Language and Environment for Statistical Computing 2012, R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/.
42. Rijpkema S.G., Molkenboer M.J., Schouls L.M., Jongejan F., Schellekens J.F. Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. J. Clin. Microbiol. 1995, 33:3091-3095.
43. Rizzoli A., Hauffe H.C., Carpi G., Vourc'h G.I., Neteler M., Rosà R. Lyme borreliosis in Europe. Eurosurveillance 2011, 16:1-8.
44. Rudenko N., Golovchenko M., Lin T., Gao L., Grubhoffer L., Oliver J.H. Delineation of a new species of the Borrelia burgdorferi sensu lato complex Borrelia americana sp. nov. J. Clin. Microbiol. 2009, 47:3875-3880.
45. Salkeld D.J., Lane R.S. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology 2010, 91:293-298.
46. Salkeld D.J., Leonhard S., Girard Y.A., Hahn N., Mum J., Padgett K.A., Lane R.S. Identifying the reservoir hosts of the Lyme disease spirochete Borrelia burgdorferi in California: the role of the Western gray squirrel (Sciurus griseus). Am. J. Trop. Med. Hyg. 2008, 79:535-540.
47. Shar S., Lkhagvasuren D., Bertolino S., Henttonen H., Kryštufek B., Meinig H. Sciurus vulgaris. IUCN 2011. IUCN Red List of Threatened Species. Version 2011.2 2008, http://www.iucnredlist.org/.
48. Skaug H., Fournier D., Nielsen A., Magnusson A., Bolker B. Generalized Linear Mixed Models using AD Model Builder 2013, R package version 0.7.2.12.
49. Skuballa J., Petney T., Pfäffle M., Oehme R., Hartelt K., Fingerle V., Kimmig P., Taraschewski H. Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe. Ticks Tick-Borne Dis. 2012, 3:8-13.
50. Slajchert T., Kitron U.D., Jones C.J., Mannelli A. Role of the Eastern chipmunk (Tamias striatus) in the epizootiology of Lyme borreliosis in Northwestern Illinois, USA. J. Wildl. Dis. 1997, 33:40-46.
51. Stanek G., Reiter M. The expanding Lyme Borrelia complex-clinical significance of genomic species?. Clin. Microbiol. Infect. 2011, 17:487-493.
52. Symonds M.R.E., Moussalli A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav. Ecol. Sociobiol. 2011, 65:13-21.
53. Venables W.N., Ripley B.D. Modern Applied Statistics with S 2002, Springer, New York, U.S.A. 4th Ed.
54. Wauters L., Bijnens L., Dhondt A.A. Body mass at weaning and juvenile recruitment in the red squirrel. J. Anim. Ecol. 1993, 62:208-286.
55. Zuur A.F., Ieno E.N., Elphick C.S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 2010, 1:3-14.
56. Zuur A.F., Ieno E.N., Walker N.J., Saveliev A.A., Smith G.M. Mixed Effects Models and Extensions in Ecology with R 2009, Springer, New York, U.S.A.
57. Zuur A.F., Saveliev A.A., Ieno E.N. Zero Inflated Models and Generalized Linear Mixed Models with R 2012, Highland Statistics Ltd., Newburgh, U.K.