Immune Resistance by Relapsing Fever Spirochetes

  • Monica E. Embers
  • Job E. Lopez
Chapter

Abstract

Relapsing fever spirochetosis is a neglected global disease primarily afflicting those in resource-poor countries (Fig. 9.1). Infection with the causative Borrelia spp. spirochetes can be either louse-borne (epidemic) or tick-borne (endemic). Signs and symptoms largely overlap, but vary between the two in important ways that affect their respective mortality. Where mortality with endemic RF is rare (<5 %), epidemic RF can reach up to 40 % mortality in an outbreak (Raoult and Roux 1999). The true global impact of this disease is masked by the non-specific symptoms caused by the spirochetal infection, such that it may be attributed to other pathogens that are prevalent in a population. For instance, in Sudan an outbreak of louse-borne relapsing fever affected 20,000 villagers with a 10 % mortality rate, yet was originally diagnosed as being caused by a hemorrhagic fever virus (Piesman and Schwan 2010). Further complicating our understanding of the potential significance of this disease is the geographical overlap of RF spirochetes with additional febrile episode-inducing illnesses (Fig. 9.1), with one study reporting that 18.2 % of RF borreliosis cases were misdiagnosed as malaria (Nordstrand et al. 2007).

References

  1. Aher AR, Shah H, Rastogi V, Tukaram PK, Choudhury RC (2008) A case report of relapsing fever. Indian J Pathol Microbiol 51(2):292–293PubMedCrossRefGoogle Scholar
  2. Alugupalli KR, Leong JM, Woodland RT, Muramatsu M, Honjo T, Gerstein RM (2004) B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21(3):379–390PubMedCrossRefGoogle Scholar
  3. Assous MV, Wilamowski A (2009) Relapsing fever borreliosis in Eurasia–forgotten, but certainly not gone! Clin Microbiol Infect 15(5):407–414PubMedCrossRefGoogle Scholar
  4. Assous MV, Wilamowski A, Bercovier H, Marva E (2006) Molecular characterization of tickborne relapsing fever Borrelia, Israel. Emerg Infect Dis 12(11):1740–1743PubMedCrossRefGoogle Scholar
  5. Balashov YS (1972) Bloodsucking ticks (Ixodoidea)- vectors of diseases of man and animals. Misc Publ Entomol Soc Am 8:161–376Google Scholar
  6. Barbour AG (1990) Antigenic variation of a relapsing fever Borrelia species. Annu Rev Microbiol 44:155–171PubMedCrossRefGoogle Scholar
  7. Barbour AG, Burman N, Carter CJ, Kitten T, Bergström S (1991) Variable antigen genes of the relapsing fever agent Borrelia hermsii are activated by promoter addition. Mol Microbiol 5:489–493PubMedCrossRefGoogle Scholar
  8. Barbour AG, Bundoc V (2001) In vitro and in vivo neutralization of the relapsing fever agent Borrelia hermsii with serotype-specific immunoglobulin M antibodies. Infect Immun 69(2): 1009–1015PubMedCrossRefGoogle Scholar
  9. Barbour AG, Carter CJ, Sohaskey CD (2000) Surface protein variation by expression site switching in the relapsing fever agent Borrelia hermsii. Infect Immun 68(12):7114–7121PubMedCrossRefGoogle Scholar
  10. Barbour AG, Dai Q, Restrepo BI, Stoenner HG, Frank SA (2006) Pathogen escape from host immunity by a genome program for antigenic variation. Proc Natl Acad Sci USA 103: 18290–18295PubMedCrossRefGoogle Scholar
  11. Battisti JM, Raffel SJ, Schwan TG (2008) A system for site-specific genetic manipulation of the relapsing fever spirochete Borrelia hermsii. Methods Mol Biol 431:69–84PubMedGoogle Scholar
  12. Breitschwerdt EB, Nicholson WL, Kiehl AR, Steers C, Meuten DJ, Levine JF (1994) Natural infections with Borrelia spirochetes in two dogs from Florida. J Clin Microbiol 32:352–357PubMedGoogle Scholar
  13. Brown RN, Lane RS (1994) Natural and experimental Borrelia burgdorferi infections in woodrats and deer mice from California. J Wildl Dis 30(3):389–398PubMedGoogle Scholar
  14. Brown RN, Peot MA, Lane RS (2006) Sylvatic maintenance of Borrelia burgdorferi (Spirochaetales) in Northern California: untangling the web of transmission. J Med Entomol 43(4):743–751PubMedCrossRefGoogle Scholar
  15. Bryceson AD, Parry EH, Perine PL, Warrell DA, Vukotich D, Leithead CS (1970) Louse-borne relapsing fever. Q J Med 39(153):129–170PubMedGoogle Scholar
  16. Burman N, Shamaei-Tousi A, Bergström S (1998) The spirochete Borrelia crocidurae causes erythrocyte rosetting during relapsing fever. Infect Immun 66:815–819PubMedGoogle Scholar
  17. Cadavid D, Bundoc V, Barbour AG (1993) Experimental infection of the mouse brain by a relapsing fever Borrelia species: a molecular analysis. J Infect Dis 168:143–151PubMedCrossRefGoogle Scholar
  18. Cadavid D, Pennington PM, Kerentseva TA, Bergström S, Barbour AG (1997) Immunologic and genetic analyses of VmpA of a neurotropic strain of Borrelia turicatae. Infect Immun 65: 3352–3360PubMedGoogle Scholar
  19. Cadavid D, Thomas DD, Crawley R, Barbour AG (1994) Variability of a bacterial surface protein and disease expression in a possible mouse model of systemic Lyme borreliosis. J Exp Med 179:631–642PubMedCrossRefGoogle Scholar
  20. Cadavid D, Barbour AG (1998) Neuroborreliosis during relapsing fever: review of the clinical manifestations, pathology, and treatment of infections in humans and experimental animals. Clin Infect Dis 26(1):151–164PubMedCrossRefGoogle Scholar
  21. Coffey EM, Eveland WC (1967) Experimental relapsing fever initiated by Borrelia hermsi. II. Sequential appearance of major serotypes in the rat. J Infect Dis 117:29–34PubMedCrossRefGoogle Scholar
  22. Connolly SE, Benach JL (2001) Cutting edge: the spirochetemia of murine relapsing fever is cleared by complement-independent bactericidal antibodies. J Immunol 167(6):3029–3032PubMedGoogle Scholar
  23. Cooley RA, Kohls GM: The Agarasidae of North America, Central America, and Cuba, Monography No. 1 edn; 1944.Google Scholar
  24. Cutler SJ (2006) Possibilities for relapsing fever reemergence. Emerg Infect Dis 12(3):369–374PubMedCrossRefGoogle Scholar
  25. Dai Q, Restrepo BI, Porcella SF, Raffel SJ, Schwan TG, Barbour AG (2006) Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol Microbiol 60:1329–1343PubMedCrossRefGoogle Scholar
  26. Davis H, Vincent JM, Lynch J (2002) Tick-borne relapsing fever caused by Borrelia turicatae. Pediatr Infect Dis J 21(7):703–705PubMedCrossRefGoogle Scholar
  27. Davis GE (1956) A relapsing fever spirochete, Borrelia mazzottii (sp. nov.) from Ornithodoros talaje from Mexico. Am J Hyg 63(1):13–17PubMedGoogle Scholar
  28. Dunham-Ems SM, Caimano MJ, Pal U, Wolgemuth CW, Eggers CH, Balic A, Radolf JD (2009) Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 119(12):3652–3665PubMedCrossRefGoogle Scholar
  29. Ehrlich PH (1910) The experimental chemotherapy of Spirilloses. Julius Springer, BerlinCrossRefGoogle Scholar
  30. Felsenfeld O (1973) The problem of relapsing fever in the Americas. IMS Ind Med Surg 42(3):7–10PubMedGoogle Scholar
  31. Fine LM, Earnhart CG, Marconi RT (2011) Genetic transformation of the relapsing fever spirochete Borrelia hermsii: stable integration and expression of green fluorescent protein from linear plasmid 200. J Bacteriol 193(13):3241–3245PubMedCrossRefGoogle Scholar
  32. Francis E (1938) Longevity of the tick Ornithodoros turicata and of Spirochaeta recurrentis with this tick. Publ Hlth Rep 53:2220–2241CrossRefGoogle Scholar
  33. Francischetti IM, Mather TN, Ribeiro JM (2003) Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochem Biophys Res Commun 305(4):869–875PubMedCrossRefGoogle Scholar
  34. Fritze D (2004) Taxonomy of the genus bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94(11):1245–1248PubMedCrossRefGoogle Scholar
  35. Grosskinsky S, Schott M, Brenner C, Cutler SJ, Kraiczy P, Zipfel PF, Simon MM, Wallich R (2009) Borrelia recurrentis employs a novel multifunctional surface protein with anti-complement, anti-opsonic and invasive potential to escape innate immunity. PLoS One 4(3):e4858PubMedCrossRefGoogle Scholar
  36. Guo BP, Teneberg S, Munch R, Terunuma D, Hatano K, Matsuoka K, Angstrom J, Boren T, Bergstrom S (2009) Relapsing fever Borrelia binds to neolacto glycans and mediates rosetting of human erythrocytes. Proc Natl Acad Sci USA 106(46):19280–19285PubMedCrossRefGoogle Scholar
  37. Guyard C, Battisti JM, Raffel SJ, Schrumpf ME, Whitney AR, Krum JG, Porcella SF, Rosa PA, DeLeo FR, Schwan TG (2006) Relapsing fever spirochetes produce a serine protease that provides resistance to oxidative stress and killing by neutrophils. Mol Microbiol 60(3): 710–722PubMedCrossRefGoogle Scholar
  38. Houhamdi L, Raoult D (2005) Excretion of living Borrelia recurrentis in feces of infected human body lice. J Infect Dis 191(11):1898–1906PubMedCrossRefGoogle Scholar
  39. Hovis KM, Freedman JC, Zhang H, Forbes JL, Marconi RT (2008) Identification of an anti-parallel coiled-coil/loop domain required for ligand binding by the Borrelia hermsii FhbA protein: additional evidence for the role of FhbA in the host-pathogen interaction. Infect Immun 76(5):2113–2122PubMedCrossRefGoogle Scholar
  40. Hovis KM, Jones JP, Sadlon T, Raval G, Gordon DL, Marconi RT (2006) Molecular analyses of the interaction of Borrelia hermsii FhbA with the complement regulatory proteins Factor H and Factor H-like protein 1. Infect Immun 74:2007–2014PubMedCrossRefGoogle Scholar
  41. Hovis KM, McDowell JV, Griffin L, Marconi RT (2004) Identification and characterization of a linear-plasmid-encoded Factor H-binding protein (FhbA) of the relapsing fever spirochete Borrelia hermsii. J Bacteriol 186:2612–2618Google Scholar
  42. Jongen VH, van Roosmalen J, Tiems J, Van Holten J, Wetsteyn JC (1997) Tick-borne relapsing fever and pregnancy outcome in rural Tanzania. Acta Obstet Gynecol Scand 76(9):834–838PubMedCrossRefGoogle Scholar
  43. Kitten T, Barbour AG (1990) Juxtaposition of expressed variable antigen genes with a conserved telomere in the bacterium Borrelia hermsii. Proc Natl Acad Sci USA 87:6077–6081Google Scholar
  44. Lawson CL, Yung BH, Barbour AG, Zuckert WR (2006) Crystal structure of neurotropism-associated variable surface protein 1 (Vsp1) of Borrelia turicatae. J Bacteriol 188(12):4522–4530PubMedCrossRefGoogle Scholar
  45. Lapierre J, Hien TV, Roose A (1971) HT, Roose A: Action de la cephaloridine dans les fievres recurrentes experimentales a Borrelia duttoni chez la souris. C R Seances Soc Biol Fil 165:282–284PubMedGoogle Scholar
  46. Lopez JE, McCoy BN, Krajacich BJ, Schwan TG (2011) Acquisition and subsequent transmission of Borrelia hermsii by the soft tick Ornithodoros hermsi. J Med Entomol 48(4):891–895PubMedCrossRefGoogle Scholar
  47. Lane RS, Brown RN (1991) Wood rats and kangaroo rats: potential reservoirs of the Lyme disease spirochete in California. J Med Entomol 28(3):299–302Google Scholar
  48. Lin T, Oliver JH Jr, Gao L, Kollars TM Jr (2001) Clark KL: Genetic heterogeneity of Borrelia burgdorferi sensu lato in the southern United States based on restriction fragment length polymorphism and sequence analysis. J Clin Microbiol 39(7):2500–2507PubMedCrossRefGoogle Scholar
  49. Larsson C, Andersson M, Pelkonen J, Guo BP, Nordstrand A, Bergstrom S (2006) Persistent brain infection and disease reactivation in relapsing fever borreliosis. Microbes Infect 8(8): 2213–2219PubMedCrossRefGoogle Scholar
  50. Leboeuf A, Gambier A (1918) Sur deux cas de spirochetose humaine a Brazzaville (Moyen Congo). Bull Soc Pathol Exot 11:359–364Google Scholar
  51. Larsson C, Andersson M, Bergstrom S (2009) Current issues in relapsing fever. Curr Opin Infect Dis 22(5):443–449PubMedCrossRefGoogle Scholar
  52. Lopez JE, Porcella SF, Schrumpf ME, Raffel SJ, Hammer CH, Zhao M, Robinson MA, Schwan TG (2009) Identification of conserved antigens for early serodiagnosis of relapsing fever Borrelia. Microbiology 155(Pt 8):2641–2651Google Scholar
  53. Lopez JE, Schrumpf ME, Nagarajan V, Raffel SJ, McCoy BN, Schwan TG (2010) A novel surface antigen of relapsing fever spirochetes can discriminate between relapsing fever and Lyme borreliosis. Clinical Vaccine Immunol 17(4):564–571CrossRefGoogle Scholar
  54. Magnarelli LA, Anderson JF, Johnson RC (1987) Cross-reactivity in serological tests for Lyme disease and other spirochetal infections. J Infect Dis 156:183–187PubMedCrossRefGoogle Scholar
  55. Malkiel S, Kuhlow CJ, Mena P, Benach JL (2009) The loss and gain of marginal zone and peritoneal B cells is different in response to relapsing fever and Lyme disease Borrelia. J Immunol 182(1):498–506PubMedGoogle Scholar
  56. Masoumi Asl H, Goya MM, Vatandoost H, Zahraei SM, Mafi M, Asmar M, Piazak N, Aghighi Z (2009) The epidemiology of tick-borne relapsing fever in Iran during 1997–2006. Travel Med Infect Dis 7(3):160–164PubMedCrossRefGoogle Scholar
  57. McCoy BN, Raffel SJ, Lopez JE, Schwan TG (2010) Bloodmeal size and spirochete acquisition of Ornithodoros hermsi (Acari: Argasidae) during feeding. J Med Entomol 47(6):1164–1172PubMedCrossRefGoogle Scholar
  58. McDowell JV, Tran E, Hamilton D, Wolfgang J, Miller K, Marconi RT (2003) Analysis of the ability of spirochete species associated with relapsing fever, avian borreliosis, and epizootic bovine abortion to bind factor H and cleave C3b. J Clin Microbiol 41:3905–3910Google Scholar
  59. Meier JT, Simon MI, Barbour AG (1985) Antigenic variation is associated with DNA rearrangements in a relapsing fever Borrelia. Cell 41:403–409PubMedCrossRefGoogle Scholar
  60. Melkert PW (1988) Relapsing fever in pregnancy: analysis of high-risk factors. Br J Obstet Gynaecol 95(10):1070–1072PubMedCrossRefGoogle Scholar
  61. Melkert PW, Stel HV (1991) Neonatal Borrelia infections (relapsing fever): report of 5 cases and review of the literature. East Afr Med J 68(12):999–1005PubMedGoogle Scholar
  62. Melkert PW (1991) Mortality in high risk patients with tick-borne relapsing fever analysed by the Borrelia-index. East Afr Med J 68(11):875–879PubMedGoogle Scholar
  63. Moemenbellah-Fard MD, Benafshi O, Rafinejad J, Ashraf H (2009) Tick-borne relapsing fever in a new highland endemic focus of western Iran. Ann Trop Med Parasitol 103(6):529–537PubMedCrossRefGoogle Scholar
  64. Mooser H (1958) Erythrocyte adhesion and hemagglomeration by relapsing fever spirochetes. Z Tropenmed Parasitol 9(2):93–111PubMedGoogle Scholar
  65. Newman K, Johnson RC (1984) T-cell-independent elimination of Borrelia turicatae. Infect Immun 45(3):572–576PubMedGoogle Scholar
  66. Nicholson WL (2002) Roles of Bacillus endospores in the environment. Cell Mol Life Sci 59(3):410–416PubMedCrossRefGoogle Scholar
  67. Nordstrand A, Bunikis I, Larsson C, Tsogbe K, Schwan TG, Nilsson M, Bergström S (2007) Tickborne relapsing fever diagnosis obscured by malaria, Togo. Emerg Infect Dis 13(1):117–123PubMedCrossRefGoogle Scholar
  68. Oliver JH Jr, Lin T, Gao L, Clark KL, Banks CW, Durden LA, James AM, Chandler FW Jr (2003) An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proc Natl Acad Sci USA 100(20):11642–11645PubMedCrossRefGoogle Scholar
  69. Pallen MJ, Wren BW (1997) The HtrA family of serine proteases. Mol Microbiol 26(2):209–221PubMedCrossRefGoogle Scholar
  70. Parola P, Raoult D (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32(6):897–928PubMedCrossRefGoogle Scholar
  71. Pennington PM, Allred CD, West CS, Alvarez R, Barbour AG (1997) Arthritis severity and spirochete burden are determined by serotype in the Borrelia turicatae-mouse model of Lyme disease. Infect Immun 65(1):285–292PubMedGoogle Scholar
  72. Pennington PM, Cadavid D, Bunikis J, Norris SJ, Barbour AG (1999a) Extensive interplasmidic duplications change the virulence phenotype of the relapsing fever agent Borrelia turicatae. Mol Microbiol 34(5):1120–1132Google Scholar
  73. Pennington PM, Cadavid D, Barbour AG (1999b) Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun 67(9):4637–4645PubMedGoogle Scholar
  74. Plasterk RHA, Simon MI, Barbour AG (1985) Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borrelia hermsii. Nature 318:257–263Google Scholar
  75. Piesman J, Mather TN, Sinsky RJ, Spielman A (1987) Duration of tick attachment and Borrelia burgdorferi transmission. J Clin Microbiol 25:557–558Google Scholar
  76. Piesman J, Schneider BS, Zeidner NS (2001) Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J Clin Microbiol 39(11):4145–4148Google Scholar
  77. Piesman J, Schwan TG (2010) Ecology of Borreliae and Their Arthropod Vectors. Caister Academic Press, Norfolk, UKGoogle Scholar
  78. Pospelova-Shtrom MV (1962) Ornithodoros ticks and their epidemiological significance. Joint Publications Research Service, DC, WashingtonGoogle Scholar
  79. Porcella SF, Raffel SJ, Schrumpf ME, Schriefer ME, Dennis DT, Schwan TG (2000) Serodiagnosis of louse-borne relapsing fever with glycerophosphodiester phosphodiesterase (GlpQ) from Borrelia recurrentis. J Clin Microbiol 38:3561–3571PubMedGoogle Scholar
  80. Ramos JM, Malmierca E, Reyes F, Tesfamariam A (2008) Results of a 10-year survey of louse-borne relapsing fever in southern Ethiopia: a decline in endemicity. Ann Trop Med Parasitol 102(5):467–469PubMedCrossRefGoogle Scholar
  81. Raoult D, Roux V (1999) The Body Louse as a Vector of Reemerging Human Diseases. Clin Infect Dis 29(4):888–911PubMedCrossRefGoogle Scholar
  82. Rawlings JA (1995) An overview of tick-borne relapsing fever with emphasis on outbreaks in Texas. Tex Med 91:56–59Google Scholar
  83. Restrepo BI, Kitten T, Carter CJ, Infante D, Barbour AG (1992) Subtelomeric expression regions of Borrelia hermsii linear plasmids are highly polymorphic. Mol Microbiol 6:3299–3311PubMedCrossRefGoogle Scholar
  84. Restrepo BI, Carter CJ, Barbour AG (1994) Activation of a vmp pseudogene in Borrelia hermsii: an alternate mechanism of antigenic variation during relapsing fever. Mol Microbiol 13:287–299PubMedCrossRefGoogle Scholar
  85. Restrepo BI, Barbour AG (1994) Antigen diversity in the bacterium B. hermsii through “somatic” mutations in rearranged vmp genes. Cell 78:867–876PubMedCrossRefGoogle Scholar
  86. Ruddy S, Austen KF (1969) C3 inactivator of man. I. Hemolytic measurement by the inactivation of cell-bound C3. J Immunol 102(3):533–543Google Scholar
  87. Ruddy S, Austen KF (1971) C3b inactivator of man. II. Fragments produced by C3b inactivator cleavage of cell-bound or fluid phase C3b. J Immunol 107(3):742–750PubMedGoogle Scholar
  88. Sarih M, Garnier M, Boudebouch N, Bouattour A, Rihani A, Hassar M, Gern L, Postic D, Cornet M (2009) Borrelia hispanica relapsing fever, Morocco. Emerg Infect Dis 15(10):1626–1629PubMedCrossRefGoogle Scholar
  89. Schwan TG, Policastro PF, Miller Z, Thompson RL, Damrow T, Keirans JE (2003) Tick-borne relapsing fever caused by Borrelia hermsii, Montana. Emerg Infect Dis 9:1151–1154PubMedCrossRefGoogle Scholar
  90. Schwan TG, Raffel SJ, Schrumpf ME, Porcella SF (2007) Diversity and distribution of Borrelia hermsii. Emerg Infect Dis 13:436–442PubMedCrossRefGoogle Scholar
  91. Schwan TG, Gage KL, Hinnebusch BJ (1995) Analysis of relapsing fever spirochetes from the western United States. J Spirochetal Tick-Borne Dis 2:3–8Google Scholar
  92. Schwan TG, Schrumpf ME, Hinnebusch BJ, Anderson DE, Konkel ME (1996) GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 34:2483–2492PubMedGoogle Scholar
  93. Schwan TG (1996) Ticks and Borrelia: model systems for investigating pathogen-arthropod interactions. Infect Agents Dis 5(3):167–181PubMedGoogle Scholar
  94. Schwan TG, Hinnebusch BJ (1998) Bloodstream- versus tick-associated variants of a relapsing fever bacterium. Science 280:1938–1940PubMedCrossRefGoogle Scholar
  95. Schwan TG, Raffel SJ, Schrumpf ME, Policastro PF, Rawlings JA, Lane RS, Breitschwerdt EB, Porcella SF (2005) Phylogenetic analysis of the spirochetes Borrelia parkeri and Borrelia turicatae and the potential for tick-borne relapsing fever in Florida. J Clin Microbiol 43: 3851–3859PubMedCrossRefGoogle Scholar
  96. Schwan TG, Raffel SJ, Schrumpf ME, Webster LS, Marques AR, Spano R, Rood M, Burns J, Hu R (2009) Tick-borne relapsing fever and Borrelia hermsii, Los Angeles County, California, USA. Emerg Infect Dis 15(7):1026–1031PubMedCrossRefGoogle Scholar
  97. Shamaei-Tousi A, Martin P, Bergh A, Burman N, Brannstrom T, Bergstrom S (1999) Erythrocyte-aggregating relapsing fever spirochete Borrelia crocidurae induces formation of microemboli. J Infect Dis 180(6):1929–1938PubMedCrossRefGoogle Scholar
  98. Shamaei-Tousi A, Collin O, Bergh A, Bergstrom S (2001) Testicular damage by microcirculatory disruption and colonization of an immune-privileged site during Borrelia crocidurae infection. J Exp Med 193(9):995–1004PubMedCrossRefGoogle Scholar
  99. Stoenner HG, Dodd T, Larsen C (1982) Antigenic variation of Borrelia hermsii. J Exp Med 156:1297–1311PubMedCrossRefGoogle Scholar
  100. Sidi G, Davidovitch N, Balicer RD, Anis E, Grotto I, Schwartz E (2005) Tickborne relapsing fever in Israel. Emerg Infect Dis 11(11):1784–1786Google Scholar
  101. Sundnes KO, Haimanot AT (1993) Epidemic of louse-borne relapsing fever in Ethiopia. Lancet 342(8881):1213–1215PubMedCrossRefGoogle Scholar
  102. Tabuchi N, Mitani H, Seino S, Fukunaga M (2002) The 44-kb linear plasmid molecule in the relapsing fever agent Borrelia duttonii strain Ly serve as a preservation of vmp genes. Microbiol Immunol 46(3):159–165Google Scholar
  103. Talbert A, Nyange A, Molteni F (1998) Spraying tick-infested houses with lambda-cyhalothrin reduces the incidence of tick-borne relapsing fever in children under five years old. Trans R Soc Trop Med Hyg 92(3):251–253PubMedCrossRefGoogle Scholar
  104. Trape JF, Duplantier JM, Bouganali H, Godeluck B, Legros F, Cornet JP, Camicas JL (1991) Tick-borne borreliosis in west Africa. Lancet 337(8739):473–475PubMedCrossRefGoogle Scholar
  105. Trape JF, Godeluck B, Diatta G, Rogier C, Legros F, Albergel J, Pepin Y, Duplantier JM (1996a) The spread of tick-borne borreliosis in West Africa and its relationship to sub-Saharan drought. Am J Trop Med Hyg 54(3):289–293PubMedGoogle Scholar
  106. Trape JF, Godeluck B, Diatta G, Rogier C, Legros F, Albergel J, Pepin Y, Duplantier JM (1996b) Tick-borne borreliosis in west Africa: recent epidemiological studies. Rocz Akad Med Bialymst 41(1):136–141PubMedGoogle Scholar
  107. van Dam AP, van Gool T, Wetsteyn JCFM, Dankert J (1999) Tick-borne relapsing fever imported from West Africa: diagnosis by quantitative buffy coat analysis and in vitro culture of Borrelia crocidurae. J Clin Microbiol 37:2027–2030PubMedGoogle Scholar
  108. Varma MGR (1962) Transmission of relapsing fever spirochetes by ticks. In: Symposia of the Zoological Society of London: 1962; Regent’s Park, London: The Zoological Society of London, 61–82Google Scholar
  109. Vaughan AT, Roghanian A, Cragg MS (2011) B cells—Masters of the immunoverse. Int J Biochem 43(3):280–285CrossRefGoogle Scholar
  110. Vial L, Diatta G, Tall A, Ba el H, Bouganali H, Durand P, Sokhna C, Rogier C, Renaud F, Trape JF (2006) Incidence of tick-borne relapsing fever in west Africa: longitudinal study. Lancet 368(9529):37–43PubMedCrossRefGoogle Scholar
  111. Vidal V, Scragg IG, Cutler SJ, Rockett KA, Fekade D, Warrell DA, Wright DJ, Kwiatkowski D (1998) Variable major lipoprotein is a principal TNF-inducing factor of louse-borne relapsing fever. Nat Med 4(12):1416–1420PubMedCrossRefGoogle Scholar
  112. Walker RL, Read DH, Hayes DC, Nordhausen RW (2002) Equine abortion associated with the Borrelia parkeri-B. turicatae tick-borne relapsing fever spirochete group. J Clin Microbiol 40:1558–1562Google Scholar
  113. Wang G, Ojaimi C, Wu H, Saksenberg V, Iyer R, Liveris D, McClain SA, Wormser GP, Schwartz I (2002) Disease severity in a murine model of lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J Infect Dis 186(6):782–791PubMedCrossRefGoogle Scholar
  114. Whitney MS, Schwan TG, Sultemeier KB, McDonald PS, Brillhart MN (2007) Spirochetemia caused by Borrelia turicatae infection in 3 dogs in Texas. Vet Clin Pathol 36(2):212–216PubMedCrossRefGoogle Scholar
  115. Yang L, Weis JH, Eichwald E, Kolbert CP, Persing DH, Weis JJ (1994) Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect Immun 62(2):492–500PubMedGoogle Scholar
  116. Zingg BC, Brown RN, Lane RS, LeFebvre RB (1993) Genetic diversity among Borrelia burgdorferi isolates from wood rats and kangaroo rats in California. J Clin Microbiol 31(12):3109–3114Google Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Monica E. Embers
    • 1
  • Job E. Lopez
    • 2
  1. 1.Division of Bacteriology and Parasitology, Tulane National Primate Research CenterTulane University Health SciencesCovingtonUSA
  2. 2.Department of Biological SciencesLee BoulevardUSA

Personalised recommendations