Occurrence and transmission efficiencies of Borrelia burgdorferi ospC types in avian and mammalian wildlife

Infection, Genetics and Evolution

Volumn 27, Issue , 2014, Pages 594-600

  Vuong, Holly B ^a,b   Canham, Charles D ^b   Fonseca, Dina M ^a   Brisson, Dustin ^c   Morin, Peter J ^a   Smouse, Peter E ^a   Ostfeld, Richard S ^b  

^a RUTGERS UNIVERSITY   (United States)

^b CARY INSTITUTE OF ECOSYSTEM STUDIES   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Likelihood model; Lyme disease; Occurrence probability; OspC; Species occupancy model; Transmission efficiency

Indexed keywords

BACTERIAL PROTEIN; OUTER SURFACE PROTEIN C; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; OSPC PROTEIN; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM DETECTION; BIRD; BORRELIA BURGDORFERI; GENOTYPE; HOST PATHOGEN INTERACTION; HOST RANGE; HOST SUSCEPTIBILITY; INFECTION RISK; MAMMAL; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; WILDLIFE; ZOONOSIS; ANIMAL; GENETICS; LYME DISEASE; MICROBIOLOGY; STATISTICAL MODEL; TRANSMISSION; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BIRDS; BORRELIA BURGDORFERI; LYME DISEASE; MODELS, STATISTICAL;

EID: 84951906681     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.12.011     Document Type: Article

References (59)

1. Alghaferi M.Y., Anderson J.M., Park J., Auwaerter P.G., Aucott J.N., Norris D.E., Dumler J.S. Borrelia burgdorferi ospC heterogeneity among human and murine isolates from a defined region of northern Maryland and southern Pennsylvania: lack of correlation with invasive and noninvasive genotypes. J. Clin. Microbiol. 2005, 43:1879-1884.
2. Anderson J.M., Norris D.E. Genetic diversity of Borrelia burgdorferi sensu stricto, in Peromyscus leucopus, the primary reservoir of Lyme disease in a region of endemicity in southern Maryland. Appl. Environ. Microbiol. 2006, 72:5331-5341.
3. Andersson M., Scherman K., Raberg L. Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity?. Am. Nat. 2013, 181:545-554.
4. Balmer O., Tanner M. Prevalence and implications of multiple-strain infections. Lancet Infect. Dis. 2011, 11:868-878.
5. Barbour A.G., Bunikis J., Travinsky B., Hoen A.G., Diuk-Wasser M.A., Fish D., Tsao J.I. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am. J. Trop. Med. Hyg. 2009, 81:1120-1131.
6. Barbour A.G., Travinsky B. Evolution and distribution of the ospC gene, a transferable serotype determinant of Borrelia burgdorferi. mBio 2010, 1.
7. Battaly G.R., Fish D. Relative importance of bird species as hosts for immature Ixodes dammini (Acari: Ixodidae) in a suburban residential landscape of southern New York state. J. Med. Entomol. 1993, 30:740-747.
8. Baum E., Hue F., Barbour A.G. Experimental infections of the reservoir species Peromyscus leucopus with diverse strains of Borrelia burgdorferi, a Lyme disease agent. mBio 2012, 3.
9. Brinkerhoff R.J., Folsom-O'Keefe C.M., Tsao K., Diuk-Wasser M.A. Do birds affect Lyme disease risk? Range expansion of the vector-borne pathogen Borrelia burgdorferi. Front. Ecol. Environ. 2011, 9:103-110.
10. Brisson D., Baxamusa N., Schwartz I., Wormser G.P. Biodiversity of Borrelia burgdorferi strains in tissues of Lyme disease patients. PLoS One 2011, 6.
11. Brisson D., Dykhuizen D.E. OspC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 2004, 168:713-722.
12. Brisson D., Dykhuizen D.E., Ostfeld R. Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proc. R. Soc. B: Biol. Sci. 2008, 275:227-235.
13. Brisson D., Vandermause M.F., Meece J.K., Reed K.D., Dykhuizen D. Evolution of northeastern and midwestern Borrelia burgdorferi, United States. Emerg. Infect. Dis. 2012, 16:911-917.
14. Burgdorfer W., Barbour A.G., Hayes S.F., Benach J.L., Grunwaldt E., Davis J.P. Lyme disease-A tick-borne spirochetosis?. Science 1982, 216:1317-1319.
15. Burnham K.P., Anderson D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2002, Springer-Verlag, New York.
16. Daniels T.J., Boccia T.M., Varde S., Marcus J., Le J., Bucher D.J., Falco R.C., Schwartz I. Geographic risk for Lyme disease and human granulocytic ehrlichiosis in southern New York State. Appl. Environ. Microbiol. 1998, 64:4663-4669.
17. Dykhuizen D.E., Brisson D., Sandigursky S., Wormser G.P., Nowakowski J., Nadelman R.B., Schwartz I. The propensity of different Borrelia burgdorferi sensu stricto genotypes to cause disseminated infections in humans. Am. J. Trop. Med. Hyg. 2008, 78:806-810.
18. Gatewood A.G., Liebman K.A., Vourc'h G., Bunikis J., Hamer S.A., Cortinas R., Melton F., Cislo P., Kitron U., Tsao J., Barbour A.G., Fish D., Diuk-Wasser M.A. Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Appl. Environ. Microbiol. 2009, 75:2476-2483.
19. Giardina A.R., Schmidt K.A., Schauber E.M., Ostfeld R.S. Modeling the role of songbirds and rodents in the ecology of Lyme disease. Can. J. Zool. 2000, 78:2184-2197.
20. Ginsberg H.S., Buckley P.A., Balmforth M.G., Zhioua E., Mitra S., Buckley F.G. Reservoir competence of native North American birds for the Lyme disease spirchete, Borrelia burgdorferi. J. Med. Entomol. 2005, 42:445-449.
21. Hamer S.A., Hickling G.J., Sidge J.L., Rosen M.E., Walker E.D., Tsao J.I. Diverse Borrelia burgdorferi strains in a bird-tick cryptic cycle. Appl. Environ. Microbiol. 2011, 77:1999-2007.
22. Hanincova 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.
23. Hanincova K., Mukherjee P., Ogden N.H., Margos G., Wormser G.P., Reed K.D., Meece J.K., Vandermause M.F., Schwartz I. Multilocus sequence typing of Borrelia burgdorferi suggests existence of lineages with differential pathogenic properties in humans. PLoS One 2013, 8:e73066.
24. Hanincova K., Ogden N.H., Diuk-Wasser M., Pappas C.J., Iyer R., Fish D., Schwartz I., Kurtenbach K. Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Appl. Environ. Microbiol. 2008, 74:153-157.
25. Hersh M.H., Tibbetts M., Strauss M., Ostfeld R.S., Keesing F. Reservoir competence of wildlife host species for Babesia microti. Emerg. Infect. Dis. 2012, 18:1951-1957.
26. Hofmeister E.K., Glass G.E., Childs J.E., Persing D.H. Population dynamics of a naturally occurring heterogeneous mixture of Borrelia burgdorferi clones. Infect. Immun. 1999, 67:5709-5716.
27. Horobik V.C., Keesing F., Ostfeld R.S. Abundance and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. Ecohealth 2006, 3:262-268.
28. Keesing F., Brunner J., Duerr S., Killilea M., LoGiudice K., Schmidt K., Vuong H., Ostfeld R.S. Hosts as ecological traps for the vector of Lyme disease. Proc. R. Soc. B-Biol. Sci. 2009, 276:3911-3919.
29. Keesing F., Hersh M.H., Tibbetts M., McHenry D.J., Duerr S., Brunner J., Killilea M., LoGiudice K., Schmidt K., Ostfeld R. Reservoir competence of vertebrate hosts for Anaplasma phagocytophilum. Emerg. Infect. Dis. 2012, 18:2013-2016.
30. Levin M.L., des Vignes F., Fish D. Disparity in the natural cycles of Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis. Emerg. Infect. Dis. 1999, 5:204-208.
31. Liang F.T., Yan J., Mbow M.L., Sviat S.L., Gilmore R.D., Mamula M., Fikrig E. Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect. Immun. 2004, 72:5759-5767.
32. LoGiudice K., Duerr S.T.K., Newhouse M.J., Schmidt K.A., Killilea M.E., Ostfeld R.S. Impact of host community composition on Lyme disease risk. Ecology 2008, 89:2841-2849.
33. 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. USA 2003, 100:567-571.
34. MacKenzie D.I., Nichols J.D., Lachman G.B., Droege S., Andrew Royle J., Langtimm C.A. Estimating site occupancy rates when detection probabilities are less than one. Ecology 2002, 83:2248-2255.
35. MacQueen D.D., Lubelczyk C., Elias S.P., Cahill B.K., Mathers A.J., Lacombe E.H., Rand P.W., Smith R.P. Genotypic diversity of an emergent population of Borrelia burgdorferi at a costal Maine island recently colonized by Ixodes scapularis. Vector Borne Zoonotic Dis. 2012, 12:456-461.
36. Margos G., Tsao J.I., Castillo-Ramirez S., Girard Y.A., Hamer S.A., Hoen A.G., Lane R.S., Raper S.L., Ogden N.H. Two boundaries separate Borrelia burgdorferi populations in North America. Appl. Environ. Microbiol. 2012, 78:6059-6067.
37. Mathers A., Smith R.P., Cahill B., Lubelczyk C., Elias S.P., Lacombe E., Morris S.R., Vary C.P., Parent C.E., Rand P.W. Strain diversity of Borrelia burgdorferi in ticks dispersed in North America by migratory birds. J. Vector Ecol. 2011, 36:24-29.
38. McCallum J. Changing use of camera traps in mammalian field research: habitats, taxa and study types. Mammal Rev. 2013, 43:196-206.
39. Murphy, L., 2012. Likelihood: methods for maximum likelihood estimation. R package v 1.5. http://CRAN.R-project.org/package=likelihood.
40. NYSDOH, 2013. New York State Department of Health: communicable diseases . http://www.health.ny.gov/statistics/diseases/communicable/.
41. Ogden N.H., Bigras-Poulin M., O'Callaghan C.J., Barker I.K., Kurtenbach K., Lindsay L.R., Charron D.F. Vector seasonality, host infection dynamics and fitness of pathogens transmitted by the tick Ixodes scapularis. Parasitology 2007, 134:209-227.
42. Ogden N.H., Lindsay L.R., Hanincova K., Barker I.K., Bigras-Poulin M., Charron D.F., Heagy A., Francis C.M., O'Callaghan C.J., Schwartz I., Thompson R.A. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl. Environ. Microbiol. 2008, 74:1780-1790.
43. Ogden N.H., Margos G., Aanensen D.M., Drebot M.A., Feil E.J., Hanincová K., Schwartz I., Tyler S., Lindsay L.R. Investigation of genotypes of Borrelia burgdorferi in Ixodes scapularis ticks collected during surveillance in Canada. Appl. Environ. Microbiol. 2011, 77:3244-3254.
44. Ohnishi J., Piesman J., de Silva A.M. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. Sci. 2001, 98:670-675.
45. Ostfeld R.S., Hazler K.R., Cepeda O.M. Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape. J. Med. Entomol. 1996, 33:90-95.
46. Qiu W.G., Bosler E.M., Campbell J.R., Ugine G.D., Wang I.N., Luft B.J., Dykhuizen D.E. A population genetic study of Borrelia burgdorferi sensu stricto from eastern Long Island, New York, suggested frequency-dependent selection, gene flow and host adaptation. Hereditas 1997, 127:203-216.
47. Qiu W.G., Dykhuizen D.E., Acosta M.S., Luft B.J. Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics 2002, 160:833-849.
48. R Core Team A Language and Environment for Statistical Computing. Version 2.15 2012, R Foundation for Statistical Computing, Vienna, Austria.
49. Rand P.W., Lacombe E.H., Smith R.P., Ficker J. Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. J. Med. Entomol. 1998, 35:270-276.
50. Richter D., Spielman A., Komar N., Matuschka F.R. Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerg. Infect. Dis. 2000, 6:133-138.
51. Scott J.D., Anderson J.F., Durden L.A. Widespread dispersal of Borrelia burgdorferi-infected ticks collected from songbirds across Canada. J. Parasitol. 2012, 98:49-59.
52. Scott J.D., Lee M.K., Fernando K., Durden L.A., Jorgensen D.R., Mak S., Morshed M.G. Detection of Lyme disease spirochete, Borrelia burgdorferi sensu lato, including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada. J. Vector Ecol. 2010, 35:124-139.
53. Seinost G., Dykhuizen D.E., Dattwyler R.J., Golde W.T., Dunn J.J., Wang I.N., Wormser G.P., Schriefer M.E., Luft B.J. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 1999, 67:3518-3524.
54. Strle K., Jones K.L., Drouin E.E., Li X., Steere A.C. Borrelia burgdorferi RST1 (OspC Type A) genotype is associated with greater inflammation and more severe Lyme disease. Am. J. Pathol. 2011, 178:2726-2739.
55. Taragel'ova V., Koci J., Hanincova K., Kurtenbach K., Derdakova M., Ogden N.H., Literak I., Kocianova E., Labuda M. Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of Borreliosis in Central Europe. Appl. Environ. Microbiol. 2008, 74:1289-1293.
56. Tsao J.I., Wootton J.T., Bunikis J., Luna M.G., Fish D., Barbour A.G. An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proc. Natl. Acad. Sci. 2004, 101:18159-18164.
57. Wang I., Dykhuizen D.E., Qui W., Dunn J.J., Bosler E.M., Luft B.J. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 1999, 151:15-30.
58. Whittaker K.A., Marzluff J.M. Species-specific survival and relative habitat use in an urban landscape during the postfledging period. Auk 2009, 126:288-299.
59. Wormser G.P., Brisson D., Liveris D., Hanincova K., Sandigursky S., Nowakowski J., Nadelman R.B., Ludin S., Schwartz I. Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J. Infect. Dis. 2008, 198:1358-1364.