Borrelia miyamotoi: A widespread tick-borne relapsing fever spirochete

Trends in Parasitology

Volumn 31, Issue 6, 2015, Pages 260-269

  Wagemakers, Alex ^a   Staarink, Pieter J ^a   Sprong, Hein ^b   Hovius, Joppe W R ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

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

Author keywords

Borrelia miyamotoi; Ixodes; Tick borne relapsing fever

Indexed keywords

ANTIBIOTIC AGENT;

ANTIBIOTIC THERAPY; BACTERIAL TRANSMISSION; BORRELIA; BORRELIA INFECTION; BORRELIA MIYAMOTOI; DISEASE CARRIER; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPROMISED PATIENT; IXODES; NONHUMAN; PREVALENCE; PUBLIC HEALTH; REVIEW; SEROPREVALENCE; SPIROCHETE INFECTION; TICK BORNE DISEASE; ANIMAL; BORRELIA INFECTIONS; PARASITE VECTOR; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; RELAPSING FEVER; TRANSMISSION;

BORRELIA BURGDORFERI GROUP; BORRELIA MIYAMOTOI; IXODES; IXODIDA; SPIROCHAETALES;

ANIMALS; ARACHNID VECTORS; BORRELIA; BORRELIA INFECTIONS; DISEASE RESERVOIRS; HUMANS; IMMUNOCOMPROMISED HOST; IXODES; RELAPSING FEVER;

EID: 84930485158     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2015.03.008     Document Type: Review

References (96)

1. Tibbles C.D., Edlow J.A. Does this patient have erythema migrans?. JAMA 2007, 297:2617-2627.
2. Joseph J.T., et al. Babesiosis in Lower Hudson Valley, New York, USA. Emerg. Infect. Dis. 2011, 17:843-847.
3. Rebaudet S., Parola P. Epidemiology of relapsing fever borreliosis in Europe. FEMS Immunol. Med. Microbiol. 2006, 48:11-15.
4. Vial L., et al. Incidence of tick-borne relapsing fever in west Africa: longitudinal study. Lancet 2006, 368:37-43.
5. Dworkin M.S., et al. The epidemiology of tick-borne relapsing fever in the United States. Am. J. Trop. Med. Hyg. 2002, 66:753-758.
6. Sarih M., et al. Borrelia hispanica relapsing fever, Morocco. Emerg. Infect. Dis. 2009, 15:1626-1629.
7. Platonov A.E., et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg. Infect. Dis. 2011, 17:1816-1823.
8. Wang G., et al. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin. Microbiol. Rev. 1999, 12:633-653.
9. Barbour A.G. Phylogeny of a relapsing fever Borrelia species transmitted by the hard tick Ixodes scapularis. Infect. Genet. Evol. 2014, 27:551-558.
10. Gupta R.S., et al. A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum. Front. Microbiol. 2013, 4:217.
11. Adeolu M., Gupta R.S. A phylogenomic and molecular marker based proposal for the division of the genus Borrelia into two genera: the emended genus Borrelia containing only the members of the relapsing fever Borrelia, and the genus Borreliella gen. nov. containing the members of the Lyme disease Borrelia (Borrelia burgdorferi sensu lato complex). Antonie Van Leeuwenhoek 2014, 105:1049-1072.
12. Scoles G.A., et al. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis. 2001, 1:21-34.
13. Elbir H., et al. African relapsing fever borreliae genomospecies revealed by comparative genomics. Front. Public Health 2014, 2:43.
14. Barbour A.G., et al. 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.
15. Takano A., et al. Characterization of reptile-associated Borrelia sp. in the vector tick, Amblyomma geoemydae, and its association with Lyme disease and relapsing fever Borrelia spp. Environ. Microbiol. Rep. 2011, 3:632-637.
16. Fukunaga M., et al. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov. isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int. J. Syst. Bacteriol. 1995, 45:804-810.
17. Stanek G., et al. Lyme borreliosis. Lancet 2012, 379:461-473.
18. Anderson J.F. Epizootiology of Borrelia in Ixodes tick vectors and reservoir hosts. Rev. Infect. Dis. 1989, 11(Suppl. 6):S1451-S1459.
19. Estrada-Pena A., Jongejan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp. Appl. Acarol. 1999, 23:685-715.
20. Hansford K.M., et al. Borrelia miyamotoi in host-seeking Ixodes ricinus ticks in England. Epidemiol. Infect. 2014, 143:1079-1087.
21. Wodecka B., et al. Host and pathogen DNA identification in blood meals of nymphal Ixodes ricinus ticks from forest parks and rural forests of Poland. Exp. Appl. Acarol. 2014, 62:543-555.
22. Dibernardo A., et al. The prevalence of Borrelia miyamotoi infection, and co-infections with other Borrelia spp. in Ixodes scapularis ticks collected in Canada. Parasit. Vectors 2014, 7:183.
23. Burri C., et al. Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum?. Ticks Tick Borne Dis. 2014, 5:245-251.
24. Wilhelmsson P., et al. Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding. Parasit. Vectors 2013, 6:362.
25. Lane R.S., et al. Eco-epidemiological factors contributing to the low risk of human exposure to ixodid tick-borne borreliae in southern California, USA. Ticks Tick Borne Dis. 2013, 4:377-385.
26. Geller J., et al. Borrelia burgdorferi sensu lato prevalence in tick populations in Estonia. Parasit. Vectors 2013, 6:202.
27. Fonville M., et al. Human exposure to tickborne relapsing fever spirochete Borrelia miyamotoi, the Netherlands. Emerg. Infect. Dis. 2014, 20:1244-1245.
28. Subramanian G., et al. Multiple tick-associated bacteria in Ixodes ricinus from Slovakia. Ticks Tick Borne Dis. 2012, 3:406-410.
29. Rosen M.E., et al. Borrelia burgdorferi not detected in widespread Ixodes scapularis (Acari: Ixodidae) collected from white-tailed deer in Tennessee. J. Med. Entomol. 2012, 49:1473-1480.
30. Richter D., et al. Absence of Lyme disease spirochetes in larval Ixodes ricinus ticks. Vector Borne Zoonotic Dis. 2012, 12:21-27.
31. Lommano E., et al. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl. Environ. Microbiol. 2012, 78:4606-4612.
32. Hamer S.A., et al. Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, U.S.A. Parasit. Vectors 2012, 5:231.
33. Wodecka B., et al. A comparative analysis of molecular markers for the detection and identification of Borrelia spirochaetes in Ixodes ricinus. J. Med. Microbiol. 2010, 59:309-314.
34. Wilhelmsson P., et al. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J. Clin. Microbiol. 2010, 48:4169-4176.
35. Tokarz R., et al. Assessment of polymicrobial infections in ticks in New York state. Vector Borne Zoonotic Dis. 2010, 10:217-221.
36. Scott M.C., et al. High-prevalence Borrelia miyamotoi infection among wild turkeys (Meleagris gallopavo) in Tennessee. J. Med. Entomol. 2010, 47:1238-1242.
37. Richter D., Matuschka F.R. Elimination of Lyme disease spirochetes from ticks feeding on domestic ruminants. Appl. Environ. Microbiol. 2010, 76:7650-7652.
38. Hoen A.G., et al. Effects of tick control by acaricide self-treatment of white-tailed deer on host-seeking tick infection prevalence and entomologic risk for Ixodes scapularis-borne pathogens. Vector Borne Zoonotic Dis. 2009, 9:431-438.
39. Fomenko N.V., et al. Diversity of Borrelia burgdorferi sensu lato in natural foci of Novosibirsk region. Int. J. Med. Microbiol. 2008, 298:139-148.
40. Richter D., Matuschka F.R. Modulatory effect of cattle on risk for Lyme disease. Emerg. Infect. Dis. 2006, 12:1919-1923.
41. Mun J., et al. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J. Med. Entomol. 2006, 43:120-123.
42. Comstedt P., et al. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg. Infect. Dis. 2006, 12:1087-1095.
43. Ullmann A.J., et al. Three multiplex assays for detection of Borrelia burgdorferi sensu lato and Borrelia miyamotoi sensu lato in field-collected Ixodes nymphs in North America. J. Med. Entomol. 2005, 42:1057-1062.
44. Richter D., et al. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg. Infect. Dis. 2003, 9:697-701.
45. Fraenkel C.J., et al. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J. Clin. Microbiol. 2002, 40:3308-3312.
46. Hovius J.W., et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 2013, 382:658.
47. Rollend L., et al. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick Borne Dis. 2013, 4:46-51.
48. Zhioua E., et al. Infection of field-collected Ixodes ricinus (Acari: Ixodidae) larvae with Borrelia burgdorferi in Switzerland. J. Med. Entomol. 1994, 31:763-766.
49. Toutoungi L.N., Gern L. Ability of transovarially and subsequent transstadially infected Ixodes hexagonus ticks to maintain and transmit Borrelia burgdorferi in the laboratory. Exp. Appl. Acarol. 1993, 17:581-586.
50. Magnarelli L.A., et al. Transovarial transmission of Borrelia burgdorferi in Ixodes dammini (Acari:Ixodidae). J. Infect. Dis. 1987, 156:234-236.
51. Lane R.S., Burgdorfer W. Transovarial and transstadial passage of Borrelia burgdorferi in the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Am. J. Trop. Med. Hyg. 1987, 37:188-192.
52. Rijpkema S., et al. Infection rates of Borrelia burgdorferi in different instars of Ixodes ricinus ticks from the Dutch North Sea Island of Ameland. Exp. Appl. Acarol. 1994, 18:531-542.
53. Stanek G., et al. Borrelia transfer by ticks during their life cycle. Studies on laboratory animals. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 1986, 263:29-33.
54. Marques A., et al. Xenodiagnosis to detect Borrelia burgdorferi infection: a first-in-human study. Clin. Infect. Dis. 2014, 58:937-945.
55. Hubalek Z., et al. Borreliae in Ixodes ricinus ticks feeding on humans. Med. Vet. Entomol. 2004, 18:228-231.
56. Taylor K.R., et al. Borrelia miyamotoi infections among wild rodents show age and month independence and correlation with Ixodes persulcatus larval attachment in Hokkaido, Japan. Vector Borne Zoonotic Dis. 2013, 13:92-97.
57. Franke J., et al. Exploring gaps in our knowledge on Lyme borreliosis spirochaetes--updates on complex heterogeneity, ecology, and pathogenicity. Ticks Tick Borne Dis. 2013, 4:11-25.
58. Medlock J.M., et al. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit. Vectors 2013, 6:1.
59. Kurtenbach K., et al. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 2006, 4:660-669.
60. Cosson J.F., et al. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasit. Vectors 2014, 7:233.
61. Hofhuis A., et al. A prospective study among patients presenting at the general practitioner with a tick bite or erythema migrans in The Netherlands. PLoS ONE 2013, 8:e64361.
62. Heyman P., et al. A clear and present danger: tick-borne diseases in Europe. Expert Rev. Anti Infect. Ther. 2010, 8:33-50.
63. Nahimana I., et al. Risk of Borrelia burgdorferi infection in western Switzerland following a tick bite. Eur. J. Clin. Microbiol. Infect. Dis. 2004, 23:603-608.
64. Huegli D., et al. Prospective study on the incidence of infection by Borrelia burgdorferi sensu lato after a tick bite in a highly endemic area of Switzerland. Ticks Tick Borne Dis. 2011, 2:129-136.
65. Fryland L., et al. Low risk of developing Borrelia burgdorferi infection in the south-east of Sweden after being bitten by a Borrelia burgdorferi-infected tick. Int. J. Infect. Dis. 2011, 15:e174-e181.
66. Tijsse-Klasen E., et al. Small risk of developing symptomatic tick-borne diseases following a tick bite in The Netherlands. Parasit. Vectors 2011, 4:17.
67. Piesman J., et al. Duration of tick attachment and Borrelia burgdorferi transmission. J. Clin. Microbiol. 1987, 25:557-558.
68. Radolf J.D., et al. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Rev. Microbiol. 2012, 10:87-99.
69. Boyle W.K., et al. Transmission dynamics of Borrelia turicatae from the arthropod vector. PLoS Negl. Trop. Dis. 2014, 8:e2767.
70. Gutierrez J., et al. Antibodies to Borrelia burgdorferi in European populations. J. Clin. Lab Anal. 2000, 14:20-26.
71. Fahrer H., et al. The prevalence and incidence of clinical and asymptomatic Lyme borreliosis in a population at risk. J. Infect. Dis. 1991, 163:305-310.
72. Carlsson S.A., et al. IgG seroprevalence of Lyme borreliosis in the population of the Aland Islands in Finland. Scand. J. Infect. Dis. 1998, 30:501-503.
73. Nohlmans M.K., et al. Prevalence of Lyme borreliosis in The Netherlands. Ned Tijdschr Geneeskd 1991, 135:2288-2292.
74. Feder H.M., et al. Persistence of serum antibodies to Borrelia burgdorferi in patients treated for Lyme disease. Clin. Infect. Dis. 1992, 15:788-793.
75. Engstrom S.M., et al. Immunoblot interpretation criteria for serodiagnosis of early Lyme disease. J. Clin. Microbiol. 1995, 33:419-427.
76. Hammers-Berggren S., et al. Serological follow-up after treatment of patients with erythema migrans and neuroborreliosis. J. Clin. Microbiol. 1994, 32:1519-1525.
77. Lee S.H., et al. Detection of borreliae in archived sera from patients with clinically suspect Lyme disease. Int. J. Mol. Sci. 2014, 15:4284-4298.
78. Schwan T.G., et al. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J. Clin. Microbiol. 1996, 34:2483-2492.
79. Porcella S.F., et al. Serodiagnosis of Louse-Borne relapsing fever with glycerophosphodiester phosphodiesterase (GlpQ) from Borrelia recurrentis. J. Clin. Microbiol. 2000, 38:3561-3571.
80. Krause P.J., et al. Human Borrelia miyamotoi infection in the United States. N. Engl. J. Med. 2013, 368:291-293.
81. Krause P.J., et al. Borrelia miyamotoi sensu lato seroreactivity and seroprevalence in the Northeastern United States. Emerg. Infect. Dis. 2014, 20:1183-1190.
82. Jahfari S., et al. High seroprevalence of Borrelia miyamotoi antibodies in forestry workers and individuals suspected of human granulocytic anaplasmosis in the Netherlands. New Microbes New Infect. 2014, 2:144-149.
83. Sato K., et al. Human infections with Borrelia miyamotoi, Japan. Emerg. Infect. Dis. 2014, 20:1391-1393.
84. Strle F., et al. Comparison of erythema migrans caused by Borrelia burgdorferi and Borrelia garinii. Vector Borne Zoonotic Dis. 2011, 11:1253-1258.
85. Chowdri H.R., et al. Borrelia miyamotoi infection presenting as human granulocytic anaplasmosis: a case report. Ann. Intern. Med. 2013, 159:21-27.
86. Gugliotta J.L., et al. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N. Engl. J. Med. 2013, 368:240-245.
87. Hue F., et al. Chromosome sequence of Borrelia miyamotoi, an uncultivable tick-borne agent of human infection. Genome Announc. 2013, 1:5.
88. Wagemakers A., 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.
89. Margos G., et al. Long-term in vitro cultivation of Borrelia miyamotoi. Ticks Tick Borne Dis. 2015, 6:181-184.
90. Parola P., et al. Tick-borne relapsing fever borreliosis, rural Senegal. Emerg. Infect. Dis. 2011, 17:883-885.
91. Kurtenbach K., et al. Host association of Borrelia burgdorferi sensu lato: the key role of host complement. Trends Microbiol. 2002, 10:74-79.
92. de Taeye S.W., et al. Complement evasion by Borrelia burgdorferi: it takes three to tango. Trends Parasitol. 2013, 29:119-128.
93. Rossmann E., et al. Dual binding specificity of a Borrelia hermsii-associated complement regulator-acquiring surface protein for factor H and plasminogen discloses a putative virulence factor of relapsing fever spirochetes. J. Immunol. 2007, 178:7292-7301.
94. Teegler A., et al. The relapsing fever spirochete Borrelia miyamotoi resists complement-mediated killing by human serum. Ticks Tick Borne Dis. 2014, 5:898-901.
95. Barbour A.G., et al. Pathogen escape from host immunity by a genome program for antigenic variation. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18290-18295.
96. Hamase A., et al. Homology of variable major protein genes between Borrelia hermsii and Borrelia miyamotoi. FEMS Microbiol. Lett. 1996, 140:131-137.