The western progression of Lyme disease: Infectious and nonclonal Borrelia burgdorferi sensu lato populations in Grand Forks County, North Dakota

Applied and Environmental Microbiology

Volumn 81, Issue 1, 2015, Pages 48-58

  Stone, Brandee L ^a   Russart, Nathan M ^b   Gaultney, Robert A ^a   Floden, Angela M ^a   Vaughan, Jefferson A ^b   Brissette, Catherine A ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; POLYMERASE CHAIN REACTION; RNA;

16S RRNA GENE; BORRELIA BURGDORFERI; INTERGENIC SPACER REGIONS; IXODES SCAPULARIS; MULTILOCUS SEQUENCE TYPING; QUANTITATIVE PCR; SEQUENCE ANALYSIS; UPPER MIDWESTS;

MAMMALS;

INFECTIOUS DISEASE; LARVA; LYME DISEASE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RNA; RODENT;

GRAND FORKS COUNTY; NORTH DAKOTA; UNITED STATES;

BORRELIA BURGDORFERI; BORRELIA BURGDORFERI GROUP; IXODES SCAPULARIS; IXODIDA; MUS; RODENTIA;

BACTERIAL DNA; BACTERIAL PROTEIN; RIBOSOME DNA; RNA 16S;

ANIMAL; ANIMAL STRUCTURES; BAGG ALBINO MOUSE; BORRELIA BURGDORFERI; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DISEASE MODEL; DISEASE TRANSMISSION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; HEART; ISOLATION AND PURIFICATION; IXODES; LYME DISEASE; MICROBIOLOGY; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; RODENT; SPIROCHETE; TICK; UNITED STATES;

ANIMAL STRUCTURES; ANIMALS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI GROUP; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, INFECTIOUS; DNA, BACTERIAL; DNA, RIBOSOMAL; GENETIC VARIATION; HEART; IXODES; LYME DISEASE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; NORTH DAKOTA; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; RODENTIA; SEQUENCE ANALYSIS, DNA; SPIROCHAETALES; TICKS;

EID: 84917692843     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02422-14     Document Type: Article

References (48)

1. Pepin KM, Eisen RJ, Mead PS, Piesman J, Fish D, Hoen AG, Barbour AG, Hamer S, Diuk-Wasser MA. 2012. Geographic variation in the relationship between human Lyme disease incidence and density of infected host-seeking Ixodes scapularis nymphs in the eastern United States. AmJ Trop Med Hyg 86:1062-1071. http://dx.doi.org/10.4269/ajtmh.2012.11-0630.
2. Minnesota Department of Health. 2013. Lyme disease in Minnesota: Lyme disease areas of highest risk. Minnesota Department of Health, St. Paul, MN.
3. Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, Cortinas R, Vourc'h G, Melton F, Hickling GJ, Tsao JI, Bunikis J, Barbour AG, Kitron U, Piesman J, Fish D. 2012. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. AmJ Trop Med Hyg 86:320-327. http://dx.doi.org/10.4269/ajtmh.2012.11-0395.
4. Russart NM, Dougherty M, Vaughan JA. 2014. Survey of ticks (Acari: Ixodidae) and tick-borne pathogens in North Dakota. J Med Entomol. 51:1087-1090. http://dx.doi.org/10.1603/ME14053.
5. North Dakota Department of Health, Division of Disease Control. 2011. Tick surveillance in North Dakota-the pump handle. North Dakota Department of Health, Division of Disease Control, Bismarck, ND.
6. Koffi JK, Leighton PA, Pelcat Y, Trudel L, Lindsay LR, Milord F, Ogden NH. 2012. Passive surveillance for I. scapularis ticks: enhanced analysis for early detection of emerging Lyme disease risk. J Med Entomol 49:400-409. http://dx.doi.org/10.1603/ME11210.
7. Rand PW, Lacombe EH, Dearborn R, Cahill B, Elias S, Lubelczyk CB, Beckett GA, Smith RP, Jr. 2007. Passive surveillance in Maine, an area emergent for tick-borne diseases. J Med Entomol 44:1118-1129. http://dx.doi.org/10.1603/0022-2585(2007)44[1118:PSIMAA]2.0.CO;2.
8. Lee X, Hardy K, Johnson DH, Paskewitz SM. 2013. Hunter-killed deer surveillance to assess changes in the prevalence and distribution of Ixodes scapularis (Acari: Ixodidae) in Wisconsin. J Med Entomol 50:632-639. http://dx.doi.org/10.1603/ME12234.
9. Bacon RM, Kugeler KJ, Mead PS. 2008. Surveillance for Lyme disease-United States, 1992-2006. MMWR Surveill Summ 57:1-9.
10. Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH, Jr. 2011. Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick-Borne Dis 2:123-128. http://dx.doi.org/10.1016/j.ttbdis.2011.04.002.
11. Strle F, Stanek G. 2009. Clinical manifestations and diagnosis of Lyme borreliosis. Curr Probl Dermatol 37:51-110. http://dx.doi.org/10.1159/000213070.
12. Clark KL, Leydet BF, Threlkeld C. 2014. Geographical and genospecies distribution of Borrelia burgdorferi sensu lato DNA detected in humans in the USA. J Med Microbiol 63:674-684. http://dx.doi.org/10.1099/jmm.0.073122-0.
13. Girard YA, Fedorova N, Lane RS. 2011. Genetic diversity of Borrelia burgdorferi and detection of B. bissettii-likeDNAin serum of north-coastal California residents. J Clin Microbiol 49:945-954. http://dx.doi.org/10.1128/JCM.01689-10.
14. Rudenko N, Golovchenko M, Rùzõek D, Piskunova N, Mallátová N, Grubhoffer L. 2009. Molecular detection of Borrelia bissettii DNA in serum samples from patients in the Czech Republic with suspected borreliosis. FEMS Microbiol Lett 292:274-281. http://dx.doi.org/10.1111/j.1574-6968.2009.01498.x.
15. Schneider BS, Schriefer ME, Dietrich G, Dolan MC, Morshed MG, Zeidner NS. 2008. Borrelia bissettii isolates induce pathology in a murine model of disease. Vector Borne Zoonotic Dis 8:623-633. http://dx.doi.org/10.1089/vbz.2007.0251.
16. Clark KL. 2013. Lyme borreliosis in human patients in Florida and Georgia, USA. Int J Med Sci 10:915-931. http://dx.doi.org/10.7150/ijms.6273.
17. Pal U, Yang X, Chen M, Bockenstedt LK, Anderson JF, Flavell RA, Norgard MV, Fikrig E. 2004. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113:220-230. http://dx.doi.org/10.1172/JCI200419894.
18. Schwan TG, Piesman J, Golde WT, Dolan MC, Rosa PA. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci U S A 92:2909-2913. http://dx.doi.org/10.1073/pnas.92.7.2909.
19. Tilly K, Krum JG, Bestor A, Jewett MW, Grimm D, Bueschel D, Byram R, Dorward D, VanRaden MJ, Stewart P, Rosa P. 2006. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 74:3554-3564. http://dx.doi.org/10.1128/IAI.01950-05.
20. Grimm D, Tilly K, Byram R, Stewart PE, Krum JG, Bueschel DM, Schwan TG, Policastro PF, Elias AF, Rosa PA. 2004. Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci U S A 101:3142-3147. http://dx.doi.org/10.1073/pnas.0306845101.
21. Seinost G, Dykhuizen DE, Dattwyler RJ, Golde WT, Dunn JJ, Wang I-N, Wormser GP, Schriefer ME, Luft BJ. 1999. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect Immun 67:3518-3524.
22. Theisen M, Borre M, Mathiesen MJ, Mikkelsen B, Lebech A-M, Hansen K. 1995. Evolution of the Borrelia burgdorferi outer surface protein OspC. J Bacteriol 177:3036-3044.
23. Lagal V, Postic D, Ruzic-Sabljic E, Baranton G. 2003. Genetic diversity among Borrelia strains determined by single-strand conformation polymorphism analysis of the ospC gene and its association with invasiveness. J Clin Microbiol 41:5059-5065. http://dx.doi.org/10.1128/JCM.41.11.5059-5065.2003.
24. Brisson D, Drecktrah D, Eggers CH, Samuels DS. 2012. Genetics of Borrelia burgdorferi. Annu Rev Genet 46:515-536. http://dx.doi.org/10.1146/annurev-genet-011112-112140.
25. Wang I-N, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, Luft BJ. 1999. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 151:15-30.
26. Wormser GP, Brisson D, Liveris D, Hanincová K, Sandigursky S, Nowakowski J, Nadelman RB, Ludin S, Schwartz I. 2008. Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J Infect Dis 198:1358-1364. http://dx.doi.org/10.1086/592279.
27. Dykhuizen DE, Brisson D, Sandigursky S, Wormser GP, Nowakowski J, Nadelman RB, Schwartz I. 2008. The propensity of different Borrelia burgdorferi sensu stricto genotypes to cause disseminated infections in humans. Am J Trop Med Hyg 78:806-810.
28. Earnhart CG, Buckles EL, Dumler JS, Marconi RT. 2005. Demonstration of OspC type diversity in invasive human Lyme disease isolates and identification of previously uncharacterized epitopes that define the specificity of the OspC murine antibody response. Infect Immun 73:7869-7877. http://dx.doi.org/10.1128/IAI.73.12.7869-7877.2005.
29. Brisson D, Dykhuizen DE. 2004. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 168:713-722. http://dx.doi.org/10.1534/genetics.104.028738.
30. Livey I, Gibbs CP, Schuster R, Dorner F. 1995. Evidence for lateral transfer and recombination in OspC variation in Lyme disease Borrelia. Mol Microbiol 18:257-269. http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_18020257.x.
31. Wang G, van Dam AP, Dankert J. 1999. Evidence for frequent OspC gene transfer between Borrelia valaisiana sp. nov. and other Lyme disease spirochetes. FEMS Microbiol Lett 177:289-296. http://dx.doi.org/10.1111/j.1574-6968.1999.tb13745.x.
32. Barbour AG, Travinsky B. 2010. Evolution and distribution of the ospC gene, a transferable serotype determinant of Borrelia burgdorferi. mBio 1:e00153-10. http://dx.doi.org/10.1128/mBio.00153-10.
33. Aanensen DM, Spratt BG. 2005. The multilocus sequence typing network: mlst.net. Nucleic Acids Res 33:W728-W733. http://dx.doi.org/10.1093/nar/gki415.
34. Margos G, Gatewood AG, Aanensen DM, Hanincová K, Terekhova D, Vollmer SA, Cornet M, Piesman J, Donaghy M, Bormane A. 2008. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc Natl Acad Sci U S A 105:8730-8735. http://dx.doi.org/10.1073/pnas.0800323105.
35. Seabloom R. 2011. White-footed mouse; deer mouse, p 305-313. In The mammals of North Dakota. North Dakota Institute for Regional Studies, Fargo, ND.
36. Barbour AG. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57:521-525.
37. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. 2004. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150:1741-1755. http://dx.doi.org/10.1099/mic.0.26944-0.
38. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633-D642. http://dx.doi.org/10.1093/nar/gkt1244.
39. Floden AM, Gonzalez T, Gaultney RA, Brissette CA. 2013. Evaluation of RevA, a fibronectin-binding protein of Borrelia burgdorferi, as a potential vaccine candidate for Lyme disease. Clin Vaccine Immunol 20:892-899. http://dx.doi.org/10.1128/CVI.00758-12.
40. Alghaferi MY, Anderson JM, Park J, Auwaerter PG, Aucott JN, Norris DE, Dumler JS. 2005. 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 43:1879-1884. http://dx.doi.org/10.1128/JCM.43.4.1879-1884.2005.
41. Steiner FE, Pinger RR, Vann CN, Grindle N, Civitello D, Clay K, Fuqua C. 2008. Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. J Med Entomol 45:289-297. http://dx.doi.org/10.1603/0022-2585(2008)45[289:IACROA]2.0.CO;2.
42. Caporale DA, Johnson CM, Millard BJ. 2005. Presence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) in southern Kettle Moraine State Forest, Wisconsin, and characterization of strain W97F51. J Med Entomol 42: 457-472. http://dx.doi.org/10.1603/0022-2585(2005)042[0457:POBBSS]2.0.CO;2.
43. Russart NM. 2013. Ticks and tick-borne pathogens in North Dakota. M.S. thesis. University of North Dakota, Grand Forks, ND.
44. Ogden NH, Lindsay LR, Hanincová K, Barker IK, Bigras-Poulin M, Charron DF, Heagy A, Francis CM, O'Callaghan CJ, Schwartz I, Thompson RA. 2008. 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 74:1780-1790. http://dx.doi.org/10.1128/AEM.01982-07.
45. Ogden NH, St-Onge L, Barker IK, Brazeau S, Bigras-Poulin M, Charron DF, Francis CM, Heagy A, Lindsay LR, Maarouf A, Michel P, Milord F, O'Callaghan CJ, Trudel L, Thompson RA. 2008. Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr 7:24. http://dx.doi.org/10.1186/1476-072X-7-24.
46. Purser JE, Norris SJ. 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci U S A 97:13865-13870. http://dx.doi.org/10.1073/pnas.97.25.13865.
47. Hinckley AF, Connally NP, Meek JI, Johnson BJ, Kemperman MM, Feldman KA, White JL, Mead PS. 2014. Lyme disease testing by large commercial laboratories in the United States. Clin Infect Dis 59:676-681. http://dx.doi.org/10.1093/cid/ciu397.
48. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275-282. http://dx.doi.org/10.1093/bioinformatics/8.3.275.