Imbalanced presence of Borrelia burgdorferi s.l. multilocus sequence types in clinical manifestations of Lyme borreliosis

Infection, Genetics and Evolution

Volumn 42, Issue , 2016, Pages 66-76

  Coipan, E Claudia ^a   Jahfari, Setareh ^a   Fonville, Manoj ^a   Oei, G Anneke ^b   Spanjaard, Lodewijk ^b   Takumi, Katsuhisa ^a   Hovius, Joppe W R ^b   Sprong, Hein ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

5S 23S rDNA intergenic spacer; Acrodermatitis chronica atrophicans; Borrelia burgdorferi s.l.; Erythema migrans; Multilocus sequence typing; Neuroborreliosis

Indexed keywords

DNA 23S; DNA 5S; SPACER DNA; RNA 23S; RNA 5S;

ACRODERMATITIS CHRONICA ATROPHICANS; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BIRD; BORRELIA; BORRELIA AFZELII; BORRELIA BAVARIENSIS; BORRELIA BURGDORFERI; BORRELIA GARINII; BORRELIA LUSITANIAE; BORRELIA SPIELMANII; BORRELIA VALAISIANA; CLINICAL FEATURE; DISEASE ASSOCIATION; EUROPE; GENETIC VARIABILITY; HAPLOTYPE; HOUSEKEEPING GENE; IXODES RICINUS; LIZARD; LYME DISEASE; MULTILOCUS SEQUENCE TYPING; NETHERLANDS; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; PREDICTION; PRIORITY JOURNAL; SPECIES DIVERSITY; SPECIES IDENTIFICATION; ZOONOSIS; ANIMAL; ARACHNID VECTOR; CLASSIFICATION; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; IXODES; MALE; MICROBIOLOGY;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI; DNA, INTERGENIC; GENOTYPE; HUMANS; IXODES; LYME DISEASE; MALE; MULTILOCUS SEQUENCE TYPING; NETHERLANDS; PHYLOGENY; RNA, RIBOSOMAL, 23S; RNA, RIBOSOMAL, 5S;

EID: 84966415530     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2016.04.019     Document Type: Article

References (70)

1. Abascal F., Zardoya R., Telford M.J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 2010, 38:W7-13.
2. Belongia E.A. Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector Borne Zoonotic Dis. (Larchmont, N.Y.) 2002, 2:265-273.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995, 57:289-300.
4. Bingsohn L., Beckert A., Zehner R., Kuch U., Oehme R., Kraiczy P., Amendt J. Prevalences of tick-borne encephalitis virus and Borrelia burgdorferi sensu lato in Ixodes ricinus populations of the Rhine-Main region, Germany. Ticks Tick Borne Dis. 2013, 4:207-213.
5. Bissett M.L., Hill W. Characterization of Borrelia burgdorferi strains isolated from Ixodes pacificus ticks in California. J. Clin. Microbiol. 1987, 25:2296-2301.
6. Brisson D., Dykhuizen D.E. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 2004, 168:713-722.
7. Burgdorfer W., Barbour A.G., Hayes S.F., Benach J.L., Grunwaldt E., Davis J.P. Lyme disease-a tick-borne spirochetosis?. Science (New York, N.Y.) 1982, 216:1317-1319.
8. Burri C., Dupasquier C., Bastic V., Gern L. Pathogens of emerging tick-borne diseases, Anaplasma phagocytophilum, Rickettsia spp., and Babesia spp., in ixodes ticks collected from rodents at four sites in Switzerland (Canton of Bern). Vector Borne Zoonotic Dis. (Larchmont, N.Y.) 2011, 11:939-944.
9. Chao A., Chazdon R.L., Colwell R.K., Shen T.-J. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol. Lett. 2005, 8:148-159.
10. Coipan E.C., Fonville M., Tijsse-Klasen E., van der Giessen J.W., Takken W., Sprong H., Takumi K. Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region. Infect. Genet. Evol. 2013, 17:216-222.
11. Coipan E.C., Jahfari S., Fonville M., Maassen C.B., van der Giessen J., Takken W., Takumi K., Sprong H. Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus. Front. Cell Infect. Microbiol. 2013, 3:36.
12. Colwell R.K. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples, Version 9 Ed 2013.
13. Colwell R.K., Coddington J.A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1994, 345:101-118.
14. Colwell R.K., Mao C.X., Chang J. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 2004, 85:2717-2727.
15. Dister S.W., Fish D., Bros S.M., Frank D.H., Wood B.L. Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. Am.J.Trop. Med. Hyg. 1997, 57:687-692.
16. 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.
17. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
18. Excoffier L., Lischer H.E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10:564-567.
19. Fingerle V., Schulte-Spechtel U.C., Ruzic-Sabljic E., Leonhard S., Hofmann H., Weber K., Pfister K., Strle F., Wilske B. Epidemiological aspects and molecular characterization of Borrelia burgdorferi s.l. from southern Germany with special respect to the new species Borrelia spielmanii sp. nov. Int. J. Med. Microbiol. 2008, 298:279-290.
20. Ginsberg H.S. Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records. Exp. Appl. Acarol. 2008, 46:29-41.
21. Glass G.E., Amerasinghe F.P., Morgan J.M., Scott T.W. Predicting Ixodes scapularis abundance on white-tailed deer using geographic information systems. Am.J.Trop. Med. Hyg. 1994, 51:538-544.
22. Glass G.E., Schwartz B.S., Morgan J.M., Johnson D.T., Noy P.M., Israel E. Environmental risk factors for Lyme disease identified with geographic information systems. Am. J. Public Health 1995, 85:944-948.
23. Glatz M., Muellegger R.R., Hizo-Teufel C., Fingerle V. Low prevalence of Borrelia bavariensis in Ixodes ricinus ticks in southeastern Austria. Ticks Tick Borne Dis. 2014, 5:649-650.
24. Gray J.S. Review the ecology of ticks transmitting Lyme borreliosis. Exp. Appl. Acarol. 1998, 22:249-258.
25. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
26. Hanincova K., Schafer S.M., Etti S., Sewell H.S., Taragelova V., Ziak D., Labuda M., Kurtenbach K. Association of Borrelia afzelii with rodents in Europe. Parasitology 2003, 126:11-20.
27. 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.
28. Haven J., Vargas L.C., Mongodin E.F., Xue V., Hernandez Y., Pagan P., Fraser-Liggett C.M., Schutzer S.E., Luft B.J., Casjens S.R., Qiu W.G. Pervasive recombination and sympatric genome diversification driven by frequency-dependent selection in Borrelia burgdorferi, the Lyme disease bacterium. Genetics 2011, 189:951-966.
29. Heylen D., Tijsse E., Fonville M., Matthysen E., Sprong H. Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ. Microbiol. 2013, 15:663-673.
30. Hoen A.G., Margos G., Bent S.J., Diuk-Wasser M.A., Barbour A., Kurtenbach K., Fish D. Phylogeography of Borrelia burgdorferi in the eastern United States reflects multiple independent Lyme disease emergence events. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:15013-15018.
31. Holden K., Hodzic E., Feng S., Freet K.J., Lefebvre R.B., Barthold S.W. Coinfection with Anaplasma phagocytophilum alters Borrelia burgdorferi population distribution in C3H/HeN mice. Infect. Immun. 2005, 73:3440-3444.
32. Hu C.M., Humair P.F., Wallich R., Gern L. Apodemus sp. rodents, reservoir hosts for Borrelia afzelii in an endemic area in Switzerland. Zentralbl. Bakteriol. 1997, 285:558-564.
33. Huegli D., Hu C.M., Humair P.F., Wilske B., Gern L. Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J. Clin. Microbiol. 2002, 40:4735-4737.
34. Hulinska D., Votypka J., Kriz B., Holinkova N., Novakova J., Hulinsky V. Phenotypic and genotypic analysis of Borrelia spp. isolated from Ixodes ricinus ticks by using electrophoretic chips and real-time polymerase chain reaction. Folia Microbiol. 2007, 52:315-324.
35. Jungnick S., Margos G., Rieger M., Dzaferovic E., Bent S.J., Overzier E., Silaghi C., Walder G., Wex F., Koloczek J., Sing A., Fingerle V. Borrelia burgdorferi sensu stricto and Borrelia afzelii: population structure and differential pathogenicity. Int. J. Med. Microbiol. 2015, 305:673-681.
36. Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 2008, 9:286-298.
37. Kimura M., Ohta T. The average number of generations until fixation of a mutant gene in a finite population. Genetics 1969, 61:763-771.
38. Kitron U., Kazmierczak J.J. Spatial analysis of the distribution of Lyme disease in Wisconsin. Am. J. Epidemiol. 1997, 145:558-566.
39. Koetsveld J., Tijsse-Klasen E., Herremans T., Hovius J.W., Sprong H. Serological and molecular evidence for spotted fever group Rickettsia and Borrelia burgdorferi sensu lato co-infections in The Netherlands. Ticks Tick Borne Dis. 2015.
40. Kuiper H., van Dam A.P., Spanjaard L., de Jongh B.M., Widjojokusumo A., Ramselaar T.C., Cairo I., Vos K., Dankert J. Isolation of Borrelia burgdorferi from biopsy specimens taken from healthy-looking skin of patients with Lyme borreliosis. J. Clin. Microbiol. 1994, 32:715-720.
41. Kurtenbach K., Hanincová 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.
42. Lommano E., Bertaiola L., Dupasquier C., Gern L. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl. Environ. Microbiol. 2012, 78:4606-4612.
43. Majlathova V., Majlath I., Derdakova M., Vichova B., Pet'ko B. Borrelia lusitaniae and green lizards (Lacerta viridis), Karst Region, Slovakia. Emerg. Infect. Dis. 2006, 12:1895-1901.
44. Mannelli A., Bertolotti L., Gern L., Gray J. Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol. Rev. 2012, 36:837-861.
45. Margos G., Gatewood A.G., Aanensen D.M., Hanincova 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.
46. 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.
47. Nicholson M.C., Mather T.N. Methods for evaluating Lyme disease risks using geographic information systems and geospatial analysis. J. Med. Entomol. 1996, 33:711-720.
48. Nieto N.C., Foley J.E. Meta-analysis of coinfection and coexposure with Borrelia burgdorferi and Anaplasma phagocytophilum in humans, domestic animals, wildlife, and Ixodes ricinus-complex ticks. Vector Borne Zoonotic Dis. (Larchmont, N.Y.) 2009, 9:93-102.
49. Oliver J.H., Lin T., Gao L., Clark K.L., Banks C.W., Durden L.A., James A.M., Chandler F.W. An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11642-11645.
50. Patterson N., Price A.L., Reich D. Population structure and eigenanalysis. PLoS Genet. 2006, 2.
51. Piesman J., Gern L. Lyme borreliosis in Europe and North America. Parasitology 2004, 129:S191-S220. (Suppl).
52. Rauter C., Hartung T. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl. Environ. Microbiol. 2005, 71:7203-7216.
53. Reik L., Burgdorfer W., Donaldson J.O. Neurologic abnormalities in Lyme disease without erythema chronicum migrans. Am. J. Med. 1986, 81:73-78.
54. Reye A.L., Hubschen J.M., Sausy A., Muller C.P. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl. Environ. Microbiol. 2010, 76:2923-2931.
55. Richter D., Matuschka F.R. Perpetuation of the Lyme disease spirochete Borrelia lusitaniae by lizards. Appl. Environ. Microbiol. 2006, 72:4627-4632.
56. Richter D., Schlee D.B., Matuschka F.R. Reservoir competence of various rodents for the Lyme disease Spirochete Borrelia spielmanii. Appl. Environ. Microbiol. 2011, 77:3565-3570.
57. Schouls L.M., Van De Pol I., Rijpkema S.G., Schot C.S. Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J. Clin. Microbiol. 1999, 37:2215-2222.
58. Stanek G., Wormser G.P., Gray J., Strle F. Lyme borreliosis. Lancet 2012, 379:461-473.
59. Stockholm, Sweden: ECDC Meeting Report. Second Expert Consultation on Tick-borne Diseases with Emphasis on Lyme Borreliosis and Tick-borne Encephalitis 2011, [updated April 2012]. (Available from: http://ecdc.europa.eu/en/publications/Publications/Tick-borne-diseases-meeting-report.pdf).
60. Strle F., Picken R.N., Cheng Y., Cimperman J., Maraspin V., Lotric-Furlan S., Ruzic-Sabljic E., Picken M.M. Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities to strain 25015. Clin. Infect. Dis. 1997, 25:273-280.
61. 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.
62. Swanson S.J., Neitzel D., Reed K.D., Belongia E.A. Coinfections acquired from ixodes ticks. Clin. Microbiol. Rev. 2006, 19:708-727.
63. Amori G., Hutterer R., Kryštufek B., Yigit N., Mitsain G., Palomo L.J. Apodemus sylvaticus. The IUCN Red List of Threatened Species 2008, IUCN, ([updated. Apodemus flavicollis Available from: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T1892A8699693 en cited 15 Nov 2015).
64. Schlitter D., van der Straeten E., Amori G., Hutterer R., Kryštufek B., Yigit N., Mitsain G. Apodemus sylvaticus. The IUCN Red List of Threatened Species 2008, IUCN, ([updated. Apodemus sylvaticus Available from: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T1904A8791394.en cited 15 Nov 2015).
65. Thomas V., Anguita J., Barthold S.W., Fikrig E. Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis alters murine immune responses, pathogen burden, and severity of Lyme arthritis. Infect. Immun. 2001, 69:3359-3371.
66. Urwin R., Maiden M.C.J. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 2003, 11:479-487.
67. van Dam A.P., Kuiper H., Vos K., Widjojokusumo A., de Jongh B.M., Spanjaard L., Ramselaar A.C., Kramer M.D., Dankert J. Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin. Infect. Dis. 1993, 17:708-717.
68. Vollmer S.A., Bormane A., Dinnis R.E., Seelig F., Dobson A.D., Aanensen D.M., James M.C., Donaghy M., Randolph S.E., Feil E.J., Kurtenbach K., Margos G. Host migration impacts on the phylogeography of Lyme Borreliosis spirochaete species in Europe. Environ. Microbiol. 2011, 13:184-192.
69. Vollmer S.A., Feil E.J., Chu C.Y., Raper S.L., Cao W.C., Kurtenbach K., Margos G. Spatial spread and demographic expansion of Lyme borreliosis spirochaetes in Eurasia. Infect. Genet. Evol. 2013, 14:147-155.
70. 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.