Relapsing Fever Borreliae: A Global Review

Clinics in Laboratory Medicine

Volumn 35, Issue 4, 2015, Pages 847-865

  Cutler, Sally J ^a  

^a UNIVERSITY OF EAST LONDON   (United Kingdom)

Author keywords

Argasid (soft) ticks; Borrelia; Clothing lice; Endemic relapsing fever; Epidemic relapsing fever; Louse borne relapsing fever; Pediculus humanus; Tick borne relapsing fever

Indexed keywords

CARBAMIC ACID DERIVATIVE; CEFTRIAXONE; CHLORAMPHENICOL; CHLORINATED HYDROCARBON; DOXYCYCLINE; ERYTHROMYCIN; INTERLEUKIN 10; ORGANOARSENIC DERIVATIVE; ORGANOPHOSPHATE; PENICILLIN DERIVATIVE; PYRETHROID; TETRACYCLINE DERIVATIVE;

BACTERIAL TRANSMISSION; BACTERIUM CULTURE; BORRELIA; BORRELIA INFECTION; CLASSIFICATION; CLINICAL FEATURE; DISEASE CARRIER; DISEASE TRANSMISSION; ECOLOGY; EPIDEMIC; HUMAN; INCIDENCE; INOCULATION; MICROBIOLOGY; MICROSCOPY; NONHUMAN; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; PROGNOSIS; PROTEOMICS; REVIEW; SEROLOGY; VECTOR CONTROL; ANIMAL; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; RELAPSING FEVER; TRANSMISSION;

ANIMALS; BORRELIA; ECOLOGY; HUMANS; PROGNOSIS; RELAPSING FEVER;

EID: 84947489138     PISSN: 02722712     EISSN: 15579832     Source Type: Journal    
DOI: 10.1016/j.cll.2015.07.001     Document Type: Review

References (100)

1. Birkhaug K., Otto H.F. Obermeier. A symposium on relapsing fever in the Americas 1942, 7-9. American Association for the Advancement of Science. Section on Medical Sciences, Washington, DC. F.R. Moulton (Ed.).
2. Bryceson A.D.M., Parry E.H.O., Perine P.L., et al. Louse-borne relapsing fever: a clinical and laboratory study of 62 cases in Ethiopia and a reconsideration of the literature. Q J Med 1970, 39:129-170.
3. Cutler S.J., Abdissa A., Trape J.F. New concepts for the old challenge of African relapsing fever borreliosis. Clin Microbiol Infect 2009, 15:400-406.
4. Schwan T.G., Anderson J.M., Lopez J.E., et al. Endemic foci of the tick-borne relapsing fever spirochete Borrelia crocidurae in Mali, West Africa, and the potential for human infection. PLoS Negl Trop Dis 2012, 6(11):e1924.
5. Ross P.H., Milne A.D. Tick fever. Br Med J 1904, ii:1453-1454.
6. Dutton J.E., Todd J.L. The nature of tick fever in the eastern part of the Congo Free State. Br Med J 1905, ii:1259-1260.
7. Mitani H., Talbert A., Fukunaga M. New World relapsing fever Borrelia found in Ornithodoros porcinus ticks in central Tanzania. Microbiol Immunol 2004, 48:501-505.
8. Naddaf S.R., Ghazinezhad B., Bahramali G., et al. Phylogenetic analysis of the spirochete Borrelia microti, a potential agent of relapsing fever in Iran. J Clin Microbiol 2012, 50:2873-2876.
9. Naddaf S., Ghazinezhad B., Sedaghat M., et al. Tickborne relapsing fever in southern Iran, 2011-2013. Emerg Infect Dis 2015, 21:1078-1080.
10. Schwan T.G., Raffel S.J., Schrumpf M.E., et al. Characterization of a novel relapsing fever spirochete in the midgut, coxal fluid, and salivary glands of the bat tick Carios kelleyi. Vector Borne Zoonotic Dis 2009, 9:643-647.
11. Yabsley M.J., Parsons N.J., Horne E.C., et al. Novel relapsing fever Borrelia detected in African penguins (Spheniscus demersus) admitted to two rehabilitation centers in South Africa. Parasitol Res 2012, 110:1125-1130.
12. Cutler S.J., Margarita Bonilla E., Singh R.J. Population structure of East African relapsing fever Borrelia spp. Emerg Infect Dis 2010, 16:1076-1080.
13. Ras N.M., Lascola B., Postic D., et al. Phylogenesis of relapsing fever Borrelia spp. Int J Syst Bacteriol 1996, 46:859-865.
14. Lescot M., Audic S., Robert C., et al. The genome of Borrelia recurrentis, the agent of deadly louse-borne relapsing fever, is a degraded subset of tick-borne Borrelia duttonii. PLoS Genet 2008, 4(9):e1000185.
15. Elbir H., Gimenez G., Robert C., et al. Complete genome sequence of Borrelia crocidurae. J Bacteriol 2012, 194:3723-3724.
16. Barbour A.G., Hayes S.F. Biology of Borrelia species. Microbiol Rev 1986, 50:381-400.
17. Bárcena-Uribarri I., Thein M., Sacher A., et al. P66 porins are present in both Lyme disease and relapsing fever spirochetes: a comparison of the biophysical properties of P66 porins from six Borrelia species. Biochim Biophys Acta 2010, 1798:1197-1203.
18. Thein M., Bunikis I., Denker K., et al. Oms38 is the first identified pore-forming protein in the outer membrane of relapsing fever spirochetes. J Bacteriol 2008, 190:7035-7042.
19. Thein M., Bonde M., Bunikis I., et al. DipA, a pore-forming protein in the outer membrane of Lyme disease spirochetes exhibits specificity for the permeation of dicarboxylates. PLoS One 2012, 7(5):e36523.
20. Magoun L., Zückert W.R., Robbins D., et al. Variable small protein (Vsp)-dependent and Vsp-independent pathways for glycosaminoglycan recognition by relapsing fever spirochaetes. Mol Microbiol 2000, 36:886-897.
21. Londoño D., Cadavid D. Bacterial lipoproteins can disseminate from the periphery to inflame the brain. Am J Pathol 2010, 176:2848-2857.
22. Guo B.P., Teneberg S., Munch R., et al. Relapsing fever Borrelia binds to neolacto glycans and mediates rosetting of human erythrocytes. Proc Natl Acad Sci U S A 2009, 106:19280-19285.
23. Shamaei-Tousi A., Martin P., Bergh A., et al. Erythrocyte-aggregating relapsing fever spirochete Borrelia crocidurae induces formation of microemboli. J Infect Dis 1999, 180:1929-1938.
24. Miller S.C., Porcella S.F., Raffel S.J., et al. Large linear plasmids of Borrelia species that cause relapsing fever. J Bacteriol 2013, 195:3629-3639.
25. Restrepo B.I., Kitten T., Carter C.J., et al. Subtelomeric expression regions of Borrelia hermsii linear plasmids are highly polymorphic. Mol Microbiol 1992, 6:3299-3311.
26. Di L., Pagan P.E., Packer D., et al. BorreliaBase: a phylogeny-centered browser of Borrelia genomes. BMC Bioinformatics 2014, 15:233.
27. Socolovschi C., Kernif T., Raoult D., et al. Borrelia, Rickettsia, and Ehrlichia species in bat ticks, France, 2010. Emerg Infect Dis 2012, 18:1966-1975.
28. Loftis A., Gill J., Schriefer M., et al. Detection of Rickettsia, Borrelia, and Bartonella in Carios kelleyi (Acari: argasidae). J Med Entomol 2005, 42:473-480.
29. Reeves W., Loftis A., Sanders F., et al. Borrelia, Coxiella, and Rickettsia in Carios capensis (Acari: Argasidae) from a brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp Appl Acarol 2006, 39:321-329.
30. Takano A., Sugimori C., Fujita H., et al. A novel relapsing fever Borrelia sp. infects the salivary glands of the molted hard tick, Amblyomma geoemydae. Ticks Tick Borne Dis 2012, 3:259-261.
31. McCoy B.N., Maïga O., Schwan T.G. Detection of Borrelia theileri in Rhipicephalus geigyi from Mali. Ticks Tick Borne Dis 2014, 5:401-403.
32. Cutler S., Abdissa A., Adamu H., et al. Borrelia in Ethiopian ticks. Ticks Tick Borne Dis 2012, 3:14-17.
33. Yparraguirre L.A., Machado-Ferreira E., Ullmann A.J., et al. A hard tick relapsing fever group spirochete in a Brazilian Rhipicephalus (Boophilus) microplus. Vector Borne Zoonotic Dis 2007, 7:717-721.
34. Kumsa B., Socolovschi C., Raoult D., et al. New Borrelia species detected in ixodid ticks in Oromia, Ethiopia. Ticks Tick Borne Dis 2015, 6:401-407.
35. Mediannikov O., Abdissa A., Socolovschi C., et al. Detection of a new Borrelia species in ticks taken from cattle in southwest Ethiopia. Vector Borne Zoonotic Dis 2013, 13:266-269.
36. Lane R.S., Mun J., Parker J.M., et al. Columbian black-tailed deer (Odocoileus hemionus columbianus) as hosts for Borrelia spp. in northern California. J Wildl Dis 2005, 41:115-125.
37. Thomas N.J., Bunikis J., Barbour A.G., et al. Fatal spirochetosis due to a relapsing fever-like Borrelia sp. in a northern spotted owl. J Wildl Dis 2002, 38:187-193.
38. Evans N., Bown K., Timofte D., et al. Fatal borreliosis in bat caused by relapsing fever spirochete, United Kingdom. Emerg Infect Dis 2009, 15:1331.
39. Trape J.F. Morbidity record in Africa for an unrecognized emergent disease. Cahiers Sante 2006, 16:102.
40. Brouqui P., Stein A., Dupont H., et al. Ectoparasitism and vector-borne diseases in 930 homeless people from Marseilles. Medicine (Baltimore) 2005, 84:61-68.
41. Li W., Ortiz G., Fournier P.-E., et al. Genotyping of human lice suggests multiple emergences of body lice from local head louse populations. PLoS Negl Trop Dis 2010, 4:e641.
42. Light J.E., Allen J.M., Long L.M., et al. Geographic distributions and origins of human head lice (Pediculus humanus capitis) based on mitochondrial data. J Parasitol 2008, 94:1275-1281.
43. Boutellis A., Mediannikov O., Bilcha K.D., et al. Borrelia recurrentis in head lice, Ethiopia. Emerg Infect Dis 2013, 19:796-798.
44. Angelakis E., Rolain J.M., Raoult D., et al. Bartonella quintana in head louse nits. FEMS Immunol Med Microbiol 2011, 62:244-246.
45. Boutellis A., Veracx A., Angelakis E., et al. Bartonella quintana in head lice from Sénégal. Vector Borne Zoonotic Dis 2012, 12:564-567.
46. Cutler S., Abdissa A., Adamu H., et al. Bartonella quintana in Ethiopian lice. Comp Immunol Microbiol Infect Dis 2012, 35:17-21.
47. Moran-Gilad J., Levine H., Schwartz E., et al. Postexposure prophylaxis of tick-borne relapsing fever: lessons learned from recent outbreaks in Israel. Vector Borne Zoonotic Dis 2013, 13:791-797.
48. Colebunders R., De Serrano P., Van Gompel A., et al. Imported relapsing fever in European tourists. Scand J Infect Dis 1993, 25:533-536.
49. Wyplosz B., Mihaila-Amrouche L., Baixench M.-T., et al. Imported tickborne relapsing fever, France. Emerg Infect Dis 2005, 11:1801-1803.
50. Rummens J.L., Louwagie A., Van Hoof A., et al. Relapsing fever imported into Belgium: a case report. Acta Clin Belg 1987, 42:210-214.
51. Kutsuna S., Kawabata H., Kasahara K., et al. Case report: the first case of imported relapsing fever in Japan. Am J Trop Med Hyg 2013, 89:460-461.
52. Schwan T.G., Policastro P.F., Miller Z., et al. Tick-borne relapsing fever caused by Borrelia hermsii, Montana. Emerg Infect Dis 2003, 9:1151-1154.
53. Trape J.F., Godeluck B., Diatta G., et al. The spread of tick-borne borreliosis in West Africa and its relationship to sub-Saharan drought. Am J Trop Med Hyg 1996, 54:289-293.
54. Cutler S.J. Relapsing fever - a forgotten disease revealed. J Appl Microbiol 2010, 108:1115-1122.
55. Nordstrand A., Bunikis I., Larsson C., et al. Tickborne relapsing fever diagnosis obscured by malaria, Togo. Emerg Infect Dis 2007, 13:117-123.
56. Diatta G., Souidi Y., Granjon L., et al. Epidemiology of tick-borne borreliosis in Morocco. PLoS Negl Trop Dis 2012, 6(9):e1810.
57. Lundqvist J., Larsson C., Nelson M., et al. Concomitant infection decreases the malaria burden but escalates relapsing fever borreliosis. Infect Immun 2010, 78:1924-1930.
58. Parola P., Diatta G., Socolovschi C., et al. Tick-borne relapsing fever borreliosis, rural Senegal. Emerg Infect Dis 2011, 17:883-885.
59. Sarih M., Garnier M., Boudebouch N., et al. Borrelia hispanica relapsing fever, Morocco. Emerg Infect Dis 2009, 15:1626-1629.
60. Schwan T.G., Raffel S.J., Schrumpf M.E., et al. Tick-borne relapsing fever and Borrelia hermsii, Los Angeles County, California, USA. Emerg Infect Dis 2009, 15:1026-1031.
61. Trevejo R.T., Schriefer M.E., Gage K.L., et al. An interstate outbreak of tick-borne relapsing fever among vacationers at a Rocky Mountain cabin. Am J Trop Med Hyg 1998, 58:743-747.
62. Ramos J.M., Malmierca E., Reyes F., et al. Results of a 10-year survey of louse-borne relapsing fever in southern Ethiopia: a decline in endemicity. Ann Trop Med Parasitol 2008, 102:467-469.
63. Cadavid D., Londoño D. Understanding tropism and immunopathological mechanisms of relapsing fever spirochaetes. Clin Microbiol Infect 2009, 15:415-421.
64. Cadavid D., Sondey M., Garcia E., et al. Residual brain infection in relapsing-fever borreliosis. J Infect Dis 2006, 193:1451-1458.
65. Mehra R., Londoño D., Sondey M., et al. Structure-function investigation of Vsp serotypes of the spirochete Borrelia hermsii. PLoS One 2009, 4(10):e7597.
66. Cadavid D., Pennington P.M., Kerentseva T.A., et al. Immunologic and genetic analyses of VmpA of a neurotropic strain of Borrelia turicatae. Infect Immun 1997, 65:3352-3360.
67. Sethi N., Sondey M., Bai Y., et al. Interaction of a neurotropic strain of Borrelia turicatae with the cerebral microcirculation system. Infect Immun 2006, 74:6408-6418.
68. Larsson C., Andersson M., Pelkonen J., et al. Persistent brain infection and disease reactivation in relapsing fever borreliosis. Microbes Infect 2006, 8:2213-2219.
69. Dai Q., Restrepo B.I., Porcella S.F., et al. Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol Microbiol 2006, 60:1329-1343.
70. Rossmann E., Kraiczy P., Herzberger P., et al. BhCRASP-1 of the relapsing fever spirochete Borrelia hermsii is a factor H- and plasminogen-binding protein. Int J Med Microbiol 2008, 298:272-283.
71. Grosskinsky S., Schott M., Brenner C., et al. Borrelia recurrentis employs a novel multifunctional surface protein with anti-complement, anti-opsonic and invasive potential to escape innate immunity. PLoS One 2009, 4(3):e4858.
72. Borgnolo G., Hailu B., Ciancarelli A., et al. Louse-borne relapsing fever. A clinical and an epidemiological study of 389 patients in Asella Hospital, Ethiopia. Trop Geogr Med 1993, 45:66-69.
73. Borgnolo G., Denku B., Chiabrera F., et al. Louse-borne relapsing fever in Ethiopian children: a clinical study. Ann Trop Paediatr 1993, 13:165-171.
74. Brown V., Larouze B., Desve G., et al. Clinical presentation of louse-born relapsing fever among Ethiopian refugees in northern Somalia. Ann Trop Med Parasitol 1988, 82:499-502.
75. Guerrier G., Doherty T. Comparison of antibiotic regimens for treating louse-borne relapsing fever: a meta-analysis. Trans R Soc Trop Med Hyg 2011, 105:483-490.
76. Negussie Y., Remick D.G., DeForge L.E., et al. Detection of plasma tumor necrosis factor, interleukins 6, and 8 during the Jarisch-Herxheimer reaction of relapsing fever. J Exp Med 1992, 175:1207-1212.
77. Fekade D., Knox K., Hussein K., et al. Prevention of Jarisch-Herxheimer reactions by treatment with antibodies against tumor necrosis factor α. N Engl J Med 1996, 335:311-315.
78. Belum G.R., Belum V.R., Chaitanya Arudra S.K., et al. The Jarisch-Herxheimer reaction: revisited. Travel Med Infect Dis 2013, 11(4):231-237.
79. Jongen V.H., van Roosmalen J., Tiems J., et al. Tick-borne relapsing fever and pregnancy outcome in rural Tanzania. Acta Obstet Gynecol Scand 1997, 76:834-838.
80. Fritz C.L., Bronson L.R., Smith C.R., et al. Isolation and characterization of Borrelia hermsii associated with two foci of tick-borne relapsing fever in California. J Clin Microbiol 2004, 42:1123-1128.
81. Larsson C., Lundqvist J., van Rooijen N., et al. A novel animal model of Borrelia recurrentis louse-borne relapsing fever borreliosis using immunodeficient mice. PLoS Negl Trop Dis 2009, 3:e522.
82. Barbour A. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 1984, 57:521-525.
83. Wagemakers A., Oei A., Fikrig M.M., et al. The relapsing fever spirochete Borrelia miyamotoi is cultivable in a modified Kelly-Pettenkofer medium, and is resistant to human complement. Parasit Vectors 2014, 7:418.
84. Cutler S.J., Jones S.E., Wright D.J.M., et al. Cultivation of East African relapsing fever Borrelia and review of preceding events. J Spirochetal Tick Borne Dis 2000, 7:52-58.
85. Cutler S.J., Akintunde C.O.K., Moss J., et al. Successful in vitro cultivation of Borrelia duttonii and its comparison with Borrelia recurrentis. Int J Syst Bacteriol 1999, 49:1793-1799.
86. Cutler S., Moss J., Fukunaga M., et al. Borrelia recurrentis characterization and comparison with relapsing fever, Lyme-associated, and other Borrelia spp. Int J Syst Bacteriol 1997, 47:958-968.
87. Cutler S.J., Fekade D., Hussein K., et al. Successful in-vitro cultivation of Borrelia recurrentis. Lancet 1994, 343:242.
88. Schwan T.G., Schrumpf M.E., Hinnebusch B.J., et al. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 1996, 34:2483-2492.
89. Lopez J., Schrumpf M., Nagarajan V., et al. A novel surface antigen of relapsing fever spirochetes can discriminate between relapsing fever and Lyme borreliosis. Clin Vaccine Immunol 2010, 17:564-571.
90. Fukunaga M., Ushijima Y., Aoki L., et al. Detection of Borrelia duttonii, a tick-borne relapsing fever agent in central Tanzania, within ticks by flagellin gene-based nested polymerase chain reaction. Vector Borne Zoonotic Dis 2001, 1:331-338.
91. Assous M.V., Wilamowski A., Bercovier H., et al. Molecular characterization of tickborne relapsing fever Borrelia, Israel. Emerg Infect Dis 2006, 12:1740-1743.
92. Elbir H., Henry M., Diatta G., et al. Multiplex real-time PCR diagnostic of relapsing fevers in Africa. PLoS Negl Trop Dis 2013, 7(1):e2042.
93. Elbir H., Gimenez G., Sokhna C., et al. Multispacer sequence typing relapsing fever borreliae in Africa. PLoS Negl Trop Dis 2012, 6(6):e1652.
94. Fotso Fotso A., Mediannikov O., Diatta G., et al. MALDI-TOF mass spectrometry detection of pathogens in vectors: the Borrelia crocidurae/Ornithodoros sonrai paradigm. PLoS Negl Trop Dis 2014, 8:e2984.
95. Talbert A., Nyange A., Molteni F. 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 1998, 92:251-253.
96. Díaz-Martín V., Manzano-Román R., Obolo-Mvoulouga P., et al. Development of vaccines against Ornithodoros soft ticks: an update. Ticks Tick Borne Dis 2015, 6:211-220.
97. D'Alessandro W.B., Humber R.A., Luz C. Occurrence of pathogenic fungi to Amblyomma cajennense in a rural area of Central Brazil and their activities against vectors of Rocky Mountain spotted fever. Vet Parasitol 2012, 188:156-159.
98. Greengarten P.J., Tuininga A.R., Morath S.U., et al. Occurrence of soil- and tick-borne fungi and related virulence tests for pathogenicity to Ixodes scapularis (Acari: Ixodidae). J Med Entomol 2011, 48:337-344.
99. Tavassoli M., Malekifard F., Soleimanzadeh A., et al. Susceptibility of different life stages of Ornithodoros lahorensis to entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Parasitol Res 2012, 111:1779-1783.
100. Assous M.V., Wilamowski A. Relapsing fever borreliosis in Eurasia - forgotten, but certainly not gone!. Clin Microbiol Infect 2009, 15:407-414.