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Borrelia miyamotoi – another emerging tick-borne pathogen


Authors: R. Kejíková 1,2;  I. Rudolf 1,2
Authors‘ workplace: Ústav biologie obratlovců AV ČR, v. v. i., Brno 1;  Ústav experimentální biologie, Přírodovědecká fakulta, Masarykova univerzita, Brno 2
Published in: Epidemiol. Mikrobiol. Imunol. 70, 2021, č. 2, s. 118-130
Category: Review Article

Overview

Borrelia miyamotoi is an emerging tick-borne pathogen phylogenetically belonging to spirochaetes causing relapsing fever. It is primarily transmitted by ticks from the Ixodes ricinus complex, similarly to borreliae causing Lyme borreliosis. Small rodents can serve as reservoir hosts. It is widespread in mild climate areas of the northern hemisphere, with constant low prevalence in ticks, in the range of units of percent. To date more than 200 human cases have been described including five cases of meningoencephalitis in immunocompromised patients. Clinical features of illness are non-specific, characterized by fever, fatigue, chills, headaches, muscles and joint pains. It can be treated with antibiotics. The diagnostic approach includes mainly PCR and serological methods. This review summarizes current knowledge on B. miyamotoi with an emphasis on taxonomy, ecology of vectors and reservoir hosts, geographical distribution, diagnosis and treatment of the disease. The review also highlights the need for an accurate determination of the etiology of the disease and its differentiation from Lyme borreliosis and human granulocytic anaplasmosis.

Keywords:

Borrelia miyamotoi – Borrelia burgdorferi – Ixodes – relapsing fever – Lyme borreliosis – vector – reservoir


Sources

1. Bouchard C, Dibernardo A, Koffi J, et al. Increased risk of tickborne diseases with climate and environmental changes. Can Commun Dis Rep, 2019;45:83–89.

2. Heyman P, Cochez Ch, Hofhuis A, et al. A clear and present danger: tick-borne diseases in Europe. Expert Rev Anti-Infect Ther, 2010;8:33–50.

3. Randolph SE. The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B-Biol Sci, 2001;356:1045–1056.

4. Fukunaga M, Takanashi Y, Tsuruta Y, 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.

5. Scoles GA, Papero M, Beati L, et al. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector-Borne Zoonotic Dis, 2001;1:21–34.

6. Fraenkel CJ, Garpmo U, Berglund J. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol, 2002;40:3308–3312.

7. Platonov AE, Karan LS, Kolyasnikova NM, et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis, 2011;17:1816–1823.

8. Krause PJ, Narasimhan S, Wormser GP, et al. Human Borrelia miyamotoi infection in the United States. N Engl J Med, 2013;368:291– 293.

9. Kadkhoda K, Dumouchel C, Brancato J, et al. Human seroprevalence of Borrelia miyamotoi in Manitoba, Canada, in 2011–2014: a cross-sectional study. CMAJ Open, 2017;5:E690–E693.

10. Jahfari S, Herremans T, Platonov AE, 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.

11. Sato K, Takano A, Konnai S, et al. Human infections with Borrelia miyamotoi, Japan. Emerg Infect Dis, 2014;20:1391–1393.

12. Jiang BG, Jia N, Jiang JF, et al. Borrelia miyamotoi infections in humans and ticks, Northeastern China. Emerg Infect Dis, 2018;24:236–241.

13. Gugliotta JL, Goethert HK, Berardi VP, et al Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N Engl J Med, 2013;368:240–245.

14. Hovius JW, de Wever B, Sohne M, et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet, 2013;382:658.

15. Boden K, Lobenstein S, Hermann B, et al. Borrelia miyamotoi-associated neuroborreliosis in immunocompromised person. Emerg Infect Dis, 2016;22:1617–1620.

16. Tobudic S, Burgmann H, Stanek G, et al. Human Borrelia miyamotoi Infection, Austria. Emerg Infect Dis, 2020;26:2201–2204.

17. Gupta SR, Mahmood S, Adeolu M. 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;4:1–17.

18. Barbour AG. Phylogeny of a relapsing fever Borrelia species transmitted by the hard tick Ixodes scapularis. Infect Genet Evol, 2014;27:551–558.

19. Bunikis J, Tsao J, Garpmo U, et al. Typing of Borrelia relapsing fever group strains. Emerg Infect Dis, 2004;10:1661–1664.

20. Cutler S, Vayssier-Taussat M, Estrada-Peña A, et al. A new Borrelia on the block: Borrelia miyamotoi – a human health risk? Euro Surveill, 2019;24(18).

21. Takano A, Goka K, Une Y, et al. Isolation and characterization of a novel Borrelia group of tick-borne borreliae from imported reptiles and their associated ticks. Environ Microbiol, 2010;12:134–146.

22. Takano A, Fujita H, Kadosaka T, 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.

23. Trinachartvanit W, Hirunkanokpun S, Sudsangiem R, et al. Borrelia sp. phylogenetically different from Lyme disease and relapsing fever-related Borrelia spp. in Amblyomma varanense from Python reticulatus. Parasites Vectors, 2016;9:359.

24. Loh SM, Gofton AW, Lo N, et al. Novel Borrelia species detected in echidna ticks, Bothriocroton concolor, in Australia. Parasites Vectors, 2016;9:339.

25. Adeolu M, Gupta RS. 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.

26. Barbour AG, Adeolu M, Gupta RS. Division of the genus Borrelia into two genera (corresponding to Lyme disease and relapsing fever groups) reflects their genetic and phenotypic distinctiveness and will lead to a better understanding of these two groups of microbes (Margos et al. (2016) There is inadequate evidence to support the division of the genus Borrelia. doi: 10.1099/ ijsem.0.001717). Int J Syst Evol Microbiol, 2017;67:2058–2067.

27. Gupta RS. Distinction between Borrelia and Borreliella is more robustly supported by molecular and phenotypic characteristics than all other neighbouring prokaryotic genera: Response to Margos‘ et al. „The genus Borrelia reloaded“ (PLoS One 13(12): e0208432). PLoS One, 2019;14:e0221397.

28. Margos G, Marosevic D, Cutler S, et al. There is inadequate evidence to support the division of the genus Borrelia. Int J Syst Evol Microbiol, 2017;67:1081–1084.

29. Margos G, Gofton A, Wibberg D, et al. The genus Borrelia reloaded. PLoS One, 2018;13:e0208432.

30. Margos G, Fingerle V, Oskam C, et al. Comment on: Gupta, 2019, distinction between Borrelia and Borreliella is more robustly supported by molecular and phenotypic characteristics than all other neighbouring prokaryotic genera: Response to Margos‘ et al. „The genus Borrelia reloaded“ (PLoS One 13(12): e0208432). PLoS One 14(8): e0221397. Ticks Tick-Borne Dis, 2020;11:101320.

31. Estrada-Peña A, Cabezas-Cruz A. Phyloproteomic and functional analyses do not support a split in the genus Borrelia (phylum Spirochaetes). BMC Evol Biol, 2019;19:54.

32. Margos G, Castillo-Ramirez S, Cutler S, et al. Rejection of the name Borreliella and all proposed species comb. nov. placed therein. Int J Syst Evol Microbiol, 2020;70:3577–3581.

33. Takano A, Toyomane K, Konnai S, et al. Tick surveillance for relapsing fever spirochete Borrelia miyamotoi in Hokkaido, Japan. PLoS One, 2014;9:e104532.

34. Mukhacheva TA, Salikhova II, Kovalev SY. Multilocus spacer analysis revealed highly homogeneous genetic background of Asian type of Borrelia miyamotoi. Infect Genet Evol, 2015;31:257–262.

35. Iwabu-Itoh Y, Bazartseren B, Naranbaatar O, et al. Tick surveillance for Borrelia miyamotoi and phylogenetic analysis of isolates in Mongolia and Japan. Ticks Tick-Borne Dis, 2017;8:850–857.

36. Krause PJ, Fish D, Narasimhan S, et al. Borrelia miyamotoi infection in nature and in humans. Clin Microbiol Infect, 2015;21:631– 639.

37. Wagemakers A, Staarink PJ, Sprong H, et al. Borrelia miyamotoi: a widespread tick-borne relapsing fever spirochete. Trends Parasitol, 2015;31:260–269.

38. Mun J, Eisen RJ, Eisen L, 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.

39. Jahfari S, Ruyts SC, Frazer-Mendelewska E, et al. Melting pot of tick-borne zoonoses: the European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas. Parasites Vectors, 2017;10:134.

40. Kim CM, Seo JW, Kim DM, et al. Detection of Borrelia miyamotoi in Ixodes nipponensis in Korea. PLoS One, 2019;14:e0220465.

41. Hamer SA, Hickling GJ, Keith R, et al. Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, U.S.A. Parasites Vectors, 2012;5:231.

42. Hauck D, Springer A, Pachnicke S, et al. Ixodes inopinatus in northern Germany: occurrence and potential vector role for Borrelia spp., Rickettsia spp., and Anaplasma phagocytophilum in comparison with Ixodes ricinus. Parasitol Res, 2019;118:3205– 3216.

43. Grech-Angelini S, Stachurski F, Vayssier-Taussat M, et al. Tickborne pathogens in ticks (Acari: Ixodidae) collected from various domestic and wild hosts in Corsica (France), a Mediterranean island environment. Transbound Emerg Dis, 2020;67:745–757.

44. Livanova NN, Fomenko NV, Akimov IA, et al. Dog survey in Russian veterinary hospitals: tick identification and molecular detection of tick-borne pathogens. Parasites Vectors, 2018;11:591.

45. Yang Y, Yang Z, Kelly P, et al. Borrelia miyamotoi sensu lato in Père David Deer and Haemaphysalis longicornis Ticks. Emerg Infect Dis, 2018;24:928–931.

46. Sprong H, Fonville M, Docters van Leeuwen A, et al. Detection of pathogens in Dermacentor reticulatus in northwestern Europe: evaluation of a high-throughput array. Heliyon, 2019;5:e01270.

47. Kohn M, Krücken J, McKay-Demeler J, et al. Dermacentor reticulatus in Berlin/Brandenburg (Germany): Activity patterns and associated pathogens. Ticks Tick-Borne Dis, 2019;10:191–206.

48. Heglasová I, Rudenko N, Golovchenko M, et al. Ticks, fleas and rodent-hosts analyzed for the presence of Borrelia miyamotoi in Slovakia: the first record of Borrelia miyamotoi in a Haemaphysalis inermis tick. Ticks Tick-Borne Dis, 2020;11:101456.

49. Han S, Lubelczyk C, Hickling GJ, et al. Vertical transmission rates of Borrelia miyamotoi in Ixodes scapularis collected from whitetailed deer. Ticks Tick-Borne Dis, 2019;10:682–689.

50. Rollend L, Fish D, Childs JE. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick-Borne Dis, 2013;4:46–51.

51. Hamer SA, Tsao JI, Walker ED, et al. Invasion of the lyme disease vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity. Ecohealth, 2010;7:47–63.

52. Hubálek Z, Halouzka J. Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitol Res, 1998;84:167–172.

53. van Duijvendijk G, Coipan C, Wagemakers A, et al. Larvae of Ixodes ricinus transmit Borrelia afzelii and B. miyamotoi to vertebrate hosts. Parasites Vectors, 2016;9:97.

54. Richter D, Debski A, Hubalek Z, et al. Absence of Lyme disease spirochetes in larval Ixodes ricinus ticks. Vector-Borne Zoonotic Dis, 2011;12:21–27.

55. Lynn GE, Breuner NE, Eisen L, et al. An immunocompromised mouse model to infect Ixodes scapularis ticks with the relapsing fever spirochete, Borrelia miyamotoi. Ticks Tick-Borne Dis, 2019;10:352–359.

56. Bunikis J, Barbour AG. Third Borrelia species in white-footed mice. Emerg Infect Dis, 2005;11:1150–1151.

57. Barbour AG, Bunikis J, Travinsky B, 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.

58. Taylor KR, Takano A, Konnai S, 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.

59. Wagemakers A, Jahfari S, de Wewer B, et al. Borrelia miyamotoi in vectors and hosts in the Netherlands. Ticks Tick-Borne Dis, 2017;8:370–374.

60. Cosson JF, Michelet L, Chotte J, et al. Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France. Parasites Vectors, 2014;7:223.

61. Hamšíková Z, Coipan C, Mahríková L, et al. Borrelia miyamotoi and co-infection with Borrelia afzelii in Ixodes ricinus ticks and rodents from Slovakia. Microb Ecol, 2017;73:1000–1008.

62. Scott MC, Rosen ME, Hamer SA, et al. High-prevalence Borrelia miyamotoi infection among wild turkeys (Meleagris gallopavo) in Tennessee. J Med Entomol, 2010;47:1238–1242.

63. Salkeld DJ, Nieto NC, Bonilla DL, et al. Borrelia miyamotoi Infections in Small Mammals, California, USA. Emerg Infect Dis, 2018;24:2356–2359.

64. Szekeres S, Docters van Leeuwen A, Tóth E, et al. Road-killed mammals provide insight into tick-borne bacterial pathogen communities within urban habitats. Transbound Emerg Dis, 2019;66:277–286.

65. Kalmár Z, Sándor AD, Matei IA, et al. Borrelia spp. in small mammals in Romania. Parasites Vectors, 2019;12:461.

66. Burri C, Schumann O, Schumann 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.

67. Wodecka B, Rymaszewska A, Skotarczak B. 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.

68. Han S, Hickling GJ, Tsao JI. High Prevalence of Borrelia miyamotoi among adult blacklegged ticks from white-tailed deer. Emerg Infect Dis, 2016;22:316–318.

69. Han S, Lubelczyk C, Hickling GJ, et al. Vertical transmission rates of Borrelia miyamotoi in Ixodes scapularis collected from whitetailed deer. Ticks Tick-Borne Dis, 2019;10:682–689.

70. Díaz P, Remesar S, Venzal JM, et al. Occurrence of Borrelia and Borreliella species in Ixodes ricinus collected from roe deer in northwestern Spain. Med Vet Entomol, 2019;33:427–430.

71. Graham ChB, Pilgard MA, Maes SE, et al. Paired real-time PCR assays for detection of Borrelia miyamotoi in North American Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae). Ticks Tick- Borne Dis, 2016;7:1230–1235.

72. Johnson TL, Graham CB, Maes SE, et al. Prevalence and distribution of seven human pathogens in host-seeking Ixodes scapularis (Acari: Ixodidae) nymphs in Minnesota, USA. Ticks Tick- Borne Dis, 2018;9:1499–1507.

73. Tokarz R, Tagliafierro T, Cucura DM, et al. Detection of Anaplasma phagocytophilum, Babesia microti, Borrelia burgdorferi, Borrelia miyamotoi and Powassan virus in ticks by a multiplex real-time reverse transcription-PCR assay. mSphere, 2017;2:e00151–17.

74. Wroblewski D, Gebhardt L, Prusinski MA, et al. Detection of Borrelia miyamotoi and other tick-borne pathogens in human clinical specimens and Ixodes scapularis ticks in New York State, 2012-2015. Ticks Tick-Borne Dis, 2017;8:407–411.

75. Xu G, Pearson P, Dykstra E, et al. Human-Biting Ixodes Ticks and Pathogen Prevalence from California, Oregon, and Washington. Vector-Borne Zoonotic Dis, 2019;19:106–114.

76. Edwards MJ, Russell JC, Davidson EN, et al. A 4 – Yr Survey of the Range of Ticks and Tick-Borne Pathogens in the Lehigh Valley Region of Eastern Pennsylvania. J Med Entomol, 2019;56:1122–1134.

77. Tokarz R, Tagliafierro T, Sameroff S, et al. Microbiome analysis of Ixodes scapularis ticks from New York and Connecticut. Ticks Tick-Borne Dis, 2019;10:894–900.

78. Sanchez-Vicente S, Tagliafierro T, Coleman JL, et al. Polymicrobial Nature of Tick-Borne Diseases. MBio, 2019;10:e02055–19.

79. Padgett K, Bonilla D, Kjemtrup A, et al. Large scale spatial risk and comparative prevalence of Borrelia miyamotoi and Borrelia burgdorferi sensu lato in Ixodes pacificus. PLoS One, 2014;9:e110853.

80. Lynn GE, Graham CB, Horiuchi K, et al. Prevalence and geographic distribution of Borrelia miyamotoi in host-seeking Ixodes pacificus (Acari: Ixodidae) nymphs in Mendocino County, California. J Med Entomol, 2018;55:711–716.

81. Dibernardo A, Cote T, Ogden NH, et al. The prevalence of Borrelia miyamotoi infection and co-infection with other Borrelia spp. in Ixodes scapularis ticks collected in Canada. Parasites Vectors, 2014;7:183.

82. Kulkarni M, Kryuchkov R, Statculescu A, et al. Ixodes scapularis tick distribution and infection rates in Ottawa, Ontario, 2017. Can Commun Dis Rep, 2018;44:237–242.

83. Rar V, Livanova N, Tkachev S, et al. Detection and genetic characterization of a wide range of infectious agents in Ixodes pavlovskyi ticks in western siberia, Russia. Parasites Vectors, 2017;10:258.

84. Rar V, Livanova N, Sabitova Y, et al. Ixodes persulcatus/pavlovskyi natural hybrids in Siberia: Occurrence in sympatric areas and infection by a wide range of tick-transmitted agents. Ticks Tick- Borne Dis, 2019;10:101254.

85. Pukhovskaya NM, Morozova OV, Vysochina NP, et al. Prevalence of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in ixodid ticks in the Far East of Russia. Int J Parasitol Parasites Wildl, 2019;8:192–202.

86. Khasnatinov MA, Danchinova GA, Takano A, et al. Prevalence of Borrelia miyamotoi in Ixodes persulcatus in Irkutsk city and its neighboring territories, Russia. Ticks Tick-Borne Dis, 2016;7:394–397.

87. Sakakibara K, Sen E, Sato K, et al. Detection and characterization off the emerging relapsing fever pathogen, Borrelia miyamotoi, from the Ixodes ricinus tick in the rural Thrakya (Thrace) region of northwest Turkey. Vector-Borne Zoonotic Dis, 2016;16:797–799.

88. Fonville M, Friesema IHM, Hengeveld PD, et al. Human exposure to tickborne relapsing fever spirochete Borrelia miyamotoi, the Netherlands. Emerg Infect Dis, 2014;20:1244–1245.

89. Cochez C, Heyman P, Heylen D, et al. The presence of Borrelia miyamotoi, a relapsing fever spirochaete, in questing Ixodes ricinus in Belgium and in The Netherlands. Zoonoses Public Health, 2015;62:331–333.

90. Michelet L, Delannoy S, Devillers E, et al. High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol, 2014;4:103.

91. Vayssier-Taussat M, Moutailler S, Michelet L, et al. Next generation sequencing uncovers unexpected bacterial pathogens in ticks in western Europe. PLoS One, 2013;8:e81439.

92. Nebbak A, Dahmana H, Almeras L, et al. Co-infection of bacteria and protozoan parasites in Ixodes ricinus nymphs collected in the Alsace region, France. Ticks Tick-Borne Dis, 2019;10:101241.

93. Szekeres S, Lügner J, Fingerle V, et al. Prevalence of Borrelia miyamotoi and Borrelia burgdorferi sensu lato in questing ticks from a recreational coniferous forest of East Saxony, Germany. Ticks Tick-Borne Dis, 2017;8:922–927.

94. Richter D, Schlee DB, Matuschka FR. Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. Emerg Infect Dis, 2003;9:697–701.

95. Crowder ChD, Carolan HE, Rounds MA, et al. Prevalence of Borrelia miyamotoi in Ixodes ticks in Europe and the United States. Emerg Infect Dis, 2014;20:1678–1682.

96. Blazejak K, Raulf MK, Janecek E, et al. Shifts in Borrelia burgdorferi (s.l.) genospecies infections in Ixodes ricinus over a 10-year surveillance period in the city of Hanover (Germany) and Borrelia miyamotoi specific Reverse Line Blot detection. Parasites Vectors, 2018;11:304.

97. Venczel R, Knoke I, Pavlovic M, et al. A novel duplex real-time PCR permits simultaneous detection and differentiation of Borrelia miyamotoi and Borrelia burgdorferi sensu lato. Infection, 2015;4:47–55.

98. Vaculová T, Derdáková M, Špitalská E, et al. Simultaneous Occurrence of Borrelia miyamotoi, Borrelia burgdorferi Sensu Lato, Anaplasma phagocytophilum and Rickettsia helvetica in Ixodes ricinus Ticks in Urban Foci in Bratislava, Slovakia. Acta Parasitol, 2019;64:19–30.

99. Subramanian G, Sekeyova Z, Raoult D, et al. Multiple tick-associated bacteria in Ixodes ricinus from Slovakia. Ticks Tick-Borne Dis, 2012;3:405–409.

100. Wilhelmsson P, Fryland L, Börjesson S, et al. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J Clin Microbiol, 2010;49:481.

101. Layzell SJ, Bailey D, Peacey M, et al. Prevalence of Borrelia burgdorferi and Borrelia miyamotoi in questing Ixodes ricinus ticks from four sites in the UK. Ticks Tick-Borne Dis, 2017;2:217–224.

102. Hansford KM, Fonville M, Jahfari S, et al. Borrelia miyamotoi in host-seeking Ixodes ricinus ticks in England. Epidemiol Infect, 2015;143:1079–1087.

103. Lambert JS, Cook MJ, Healy JE, et al. Metagenomic 16S rRNA gene sequencing survey of Borrelia species in Irish samples of Ixodes ricinus ticks. PLoS One, 2019;14:e0209881.

104. Kiewra D, Stanczak J, Richter M. Ixodes ricinus (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in Lower Silesia, Poland – preliminary study. Ticks Tick-Borne Dis, 2014;5:892–897.

105. Kubiak K, Dziekońska-Rynko J, Szymańska H, et al. Questing Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in an urban area of north-eastern Poland. Exp Apl Acarol, 2019;78:113–126.

106. Reiter M, Schötta AM, Müller A, et al. A newly established real- time PCR for detection of Borrelia miyamotoi in Ixodes ricinus ticks. Ticks Tick-Borne Dis, 2015;6:303–308.

107. Ruyts SC, Tack W, Ampoorter E, et al. Year-to-year variation in the density of Ixodes ricinus ticks and the prevalence of the rodent-associated human pathogens Borrelia afzelii and B. miyamotoi in different forest types. Ticks Tick-Borne Dis, 2018;9:141–145.

108. Szerekes S, Coipan EC, Rigó K, et al. Eco-epidemiology of Borrelia miyamotoi in a popular hunting and recreational forest area in Hungary. Parasites Vectors, 2015;8:309.

109. Diaz P, Arnal LJ, Remesar S, et al. Molecular identification of Borrelia spirochetes in questing Ixodes ricinus from northwest Spain. Parasites Vectors, 2017;10:615.

110. Remesar S, Díaz P, Venzal JM, et al. Longitudinal Study of Infection with Borrelia spp. in Questing Ticks from North-Western Spain. Vector-Borne Zoonotic Dis, 2019;19:785–792.

111. Klitgaard K, Højgaard J, Isbrand A, et al. Screening for multiple tick-borne pathogens in Ixodes ricinus ticks from birds in Denmark during spring and autumn migration seasons. Ticks Tick- Borne Dis, 2019;10:546–552.

112. Kjelland V, Rollum R, Korslund L, et al. Borrelia miyamotoi is widespread in Ixodes ricinus ticks in southern Norway. Ticks Tick- Borne Dis, 2015;6:516–521.

113. Kjelland V, Paulsen KM, Rollum R, et al. Tick-borne encephalitis virus, Borrelia burgdorferi sensu lato, Borrelia miyamotoi, Anaplasma phagocytophilum and Candidatus Neoehrlichia mikurensis in Ixodes ricinus ticks collected from recreational islands in southern Norway. Ticks Tick-Borne Dis, 2018;9:1098–1102.

114. Geller J, Nazarova L, Katargina O, et al. Detection and genetic characterization of relapsing fever spirochete Borrelia miyamotoi in Estonian ticks. PLoS One, 2012;7:e51914.

115. Potkonjak A, Kleinerman G, Gutiérrez R, et al. Occurence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks with first identification of Borrelia miyamotoi in Vojvodina, Serbia. Vector-Borne Zoonotic Dis, 2016;16:631–635.

116. Rogovskyy A, Batool M, Gillis DC, et al. Diversity of Borrelia spirochetes and other zoonotic agents in ticks from Kyiv, Ukraine. Ticks Tick-Borne Dis, 2018;9:404–409.

117. Ravagnan S, Tomassone L, Montarsi F, et al. First detection of Borrelia miyamotoi in Ixodes ricinus ticks from northern Italy. Parasites Vectors, 2018;11:130.

118. Andersson MO, Marga G, Banu T, et al. Tick-borne pathogens in tick species infesting humans in Sibiu County, central Romania. Parasitol Res, 2018;117:1591–1597.

119. Sormunen JJ, Klemola T, Hänninen J, et al. The importance of study duration and spatial scale in pathogen detection- -evidence from a tick-infested island. Emerg Microbes Infect, 2018;7:189.

120. Namina A, Capligina V, Seleznova M, et al. Tick-borne pathogens in ticks collected from dogs, Latvia, 2011–2016. BMC Vet Res, 2019;15:398.

121. Hamer SA, Hickling GJ, Walker ED, et al. Increased diversity of zoonotic pathogens and Borrelia burgdorferi strains in established versus incipient Ixodes scapularis populations across the Midwestern United States. Infect Genet Evol, 2014;27:531–542.

122. Hulínská D, Votýpka J, Kríz B, et al. 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.

123. Hájková H. Výskyt klíšťat a analýza jimi přenášených druhů borelie v rekreačních zónách v Českých Budějovicích a okolí. Mapovaní výskytu B. miyamotoi v klíšťatech z vybraných regionů Jižních Čech. Bakalářská práce, Jihočeská univerzita v Českých Budějovicích, České Budějovice. 2014; 26 s.

124. Honig V, Carolan HE, Vavruskova Z, et al. Broad-range survey of vector-borne pathogens and tick host identification of Ixodes ricinus from Southern Czech Republic. FEMS Microbiol Ecol, 2017;93:1–13.

125. Telford SR, Goethert HK, Molloy PJ, et al. Borrelia miyamotoi disease: neither Lyme disease nor relapsing fever. Clin Lab Med, 2015;35:867–882.

126. Krause PJ, Schwab J, Narasimhan S, et al. Hard tick relapsing fever caused by Borrelia miyamotoi in a child. Pediatr Infect Dis J, 2016;35:1352–1354.

127. Sarksyan DS, Platonov AE, Karan LS, et al. Probability of spirochete Borrelia miyamotoi transmission from ticks to humans. Emerg Infect Dis, 2015;21:2273–2274.

128. Fiorito TM, Reece R, Flanigan TP, et al. Borrelia miyamotoi polymerase chain reaction positivity on a tick-borne disease panel in an endemic region of Rhode Island: a case series. Infect Dis Clin Pract, 2017;25:250–254.

129. Molloy PJ, Telford SR 3rd, Chowdri HR, et al. Borrelia miyamotoi disease in the northeastern United States: a case series. Ann Intern Med, 2015;163:91–98.

130. Chowdri HR, Gugliotta JL, Berardi VP, et al. Borrelia miyamotoi infection presenting as human granulocytic anaplasmosis: a case report. Ann Intern Med, 2013;159:21–27.

131. Sudhindra P, Wang G, Schriefer ME, et al. Insights into Borrelia miyamotoi infection from an untreated case demonstrating relapsing fever, monocytosis and positive C6 Lyme serology. Diagn Microbiol Infect Dis, 2016;86:93–96.

132. Jobe DA, Lovrich SD, Oldenburg DG, et al. Borrelia miyamotoi Infection in Patients from Upper Midwestern United States, 2014–2015. Emerg Infect Dis, 2016;22:1471–1473.

133. Hoornstra D, Koetsveld J, Sprong H, et al. Borrelia miyamotoi Disease in an Immunocompetent Patient, Western Europe. Emerg Infect Dis, 2018;24:1770–1772.

134. Oda R, Kutsuna S, Sekikawa Y, et al. The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease. J Infect Chemother, 2017;23:333–335.

135. Franck M, Ghozzi R, Pajaud J, et al. Borrelia miyamotoi: 43 Cases Diagnosed in France by Real-Time PCR in Patients With Persistent Polymorphic Signs and Symptoms. Front Med (Lausanne), 2020;7:55.

136. Siński E, Welc-Falęciak R, Zajkowska J. Borrelia miyamotoi: A human tick-borne relapsing fever spirochete in Europe and its potential impact on public health. Adv Med Sci, 2016;61:255– 260.

137. Krause PJ, Narasimhan S, Wormser GP, et al. Borrelia miyamotoi sensu lato seroreactivity and seroprevalence in the northeastern United States. Emerg Infect Dis, 2014;20:1183–1190.

138. Krause PJ, Carroll M, Fedorova N, et al. Human Borrelia miyamotoi infection in California: serodiagnosis is complicated by multiple endemic Borrelia species. PLoS One, 2018;13:e0191725.

139. Smith RP Jr., Elias SP, Cavanaugh CE, et al. Seroprevalence of Borrelia burgdorferi, B. miyamotoi, and Powassan Virus in Residents Bitten by Ixodes Ticks, Maine, USA. Emerg Infect Dis, 2019;25:804–807.

140. Sato K, Sakakibara K, Masuzawa T, et al. Case control study: Serological evidence that Borrelia miyamotoi disease occurs nationwide in Japan. J Infect Chemother, 2018;24:828–833.

141. Henningsson AJ, Asgeirsson H, Hammas B, et al. Two Cases of Borrelia miyamotoi Meningitis, Sweden, 2018. Emerg Infect Dis, 2019;25:1965–1968.

142. Krause PJ, Hendrickson JE, Steeves TK, et al. Blood transfusion transmission of the tick-borne relapsing fever spirochete Borrelia miyamotoi in mice. Transfusion, 2015;55:593–597.

143. Thorp AM, Tonnetti L. Distribution and survival of Borrelia miyamotoi in human blood components. Transfusion, 2016;56:705–711.

144. Koetsveld J, Draga ROP, Wagemakers A, et al. In vitro susceptibility of the relapsing-fever spirochete Borrelia miyamotoi to antimicrobial agents. Antimicrob Agents Chemother, 2017;61:e00535–17.

145. Koetsveld J, Manger A, Hoornstra D, et al. In Vitro Antimicrobial Susceptibility of Clinical Isolates of Borrelia miyamotoi. Antimicrob Agents Chemother, 2018;62:e00419–18.

146. Telford SR, Goethert HK, Molloy PJ, et al. Blood Smears Have Poor Sensitivity for Confirming Borrelia miyamotoi Disease. J Clin Microbiol, 2019;57:e01468–18.

147. Barbour AG. Isolation and cultivation of Lyme disease spirochaetes. Yale J Biol Med, 1984;57:521–525.

148. Margos G, Stockmeier S, Hizo-Teufel C, et al. Long-term in vitro cultivation of Borrelia miyamotoi. Ticks Tick-Borne Dis, 2015;6:181–184.

149. Stone BL, Brissette CA. Laboratory cultivation and maintenance of Borrelia miyamotoi. Curr Protoc Microbiol, 2016;42:12F.1.1– 12F.1.6.

150. Wagemakers A, Oei A, Fikrig MM, et al. The relapsing fever spirochete Borrelia miyamotoi is cultivable in a modified Kelly-Pettenkofer medium, and is resistant to human complement. Parasites Vectors, 2014;7:418.

151. Koetsveld J, Kolyasnikova NM, Wagemakers A, et al. Development and optimization of an in vitro cultivation protocol allows for isolation of Borrelia miyamotoi from patients with hard tickborne relapsing fever. Clin Microbiol Infect, 2017;23:480–484.

152. Schwan TG, Schrumpf ME, Hinnebusch BJ, et al. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol, 1996;34:2483–2492.

153. Karan L, Makenov M, Kolyasnikova N, et al. Dynamics of Spirochetemia and Early PCR Detection of Borrelia miyamotoi. Emerg Infect Dis, 2018;24:860–867.

154. Hue F, Langeroudi AG, Barbour AG. Chromosome sequence of Borrelia miyamotoi, an uncultivable tick-borne agent of human infection. Genome Announc, 2013;1:e00713–13.

155. Kingry LC, Replogle A, Batra D, et al. Toward a Complete North American Borrelia miyamotoi Genome. Genome Announc, 2017;5:e01557–16.

156. Kingry LC, Replogle A, Dolan M, et al. Chromosome and Large Linear Plasmid Sequences of a Borrelia miyamotoi Strain Isolated from Ixodes pacificus Ticks from California. Genome Announc, 2017;5:e00960–17.

157. Kuleshov KV, Koetsveld J, Goptar IA, et al. Whole-Genome Sequencing of Six Borrelia miyamotoi Clinical Strains Isolated in Russia. Genome Announc, 2018;6:e01424–17.

158. Kuleshov KV, Hoornstra D, Sprong H, et al. Draft Whole-Genome Sequences of Two Western European Borrelia miyamotoi Isolates. Microbiol Resour Announc, 2019;8:e01314–19.

159. Janeček J, Nováková M, Oppelt J, et al. Complete Chromosomal Sequences of Two Borrelia miyamotoi Samples Obtained from Ixodes ricinus Eggs in Czechia. Microbiol Resour Announc, 2020;9:e01504–19.

160. Wagemakers A, Koetsveld J, Narasimhan S, et al. Variable Major Proteins as Targets for Specific Antibodies against Borrelia miyamotoi. J Immunol, 2016;196:4185–4195.

161. Koetsveld J, Kolyasnikova NM, Wagemakers A, et al. Serodiagnosis of Borrelia miyamotoi disease by measuring antibodies against GlpQ and variable major proteins. Clin Microbiol Infect, 2018;24:1338.e1–1338.e7.

162. Jahfari S, Sarksyan DS, Kolyasnikova NM, et al. Evaluation of a serological test for the diagnosis of Borrelia miyamotoi disease in Europe. J Microbiol Methods, 2017;136:11–16.

163. Tokarz R, Tagliafierro T, Caciula A, et al. Identification of immunoreactive linear epitopes of Borrelia miyamotoi. Ticks Tick-Borne Dis, 2020;11:101314.

164. Lee SH, Vigliotti JS, Vigliotti VS, et al. Detection of borreliae in archived sera from patients with clinically suspect Lyme disease. Int J Mol Sci, 2014;15:4284–4298.

165. Molloy PJ, Weeks KE, Todd B, et al. Seroreactivity to the C6 Peptide in Borrelia miyamotoi Infections Occurring in the Northeastern United States. Clin Infect Dis, 2018;66:1407–1410.

166. Koetsveld J, Platonov AE, Kuleshov K, et al. Borrelia miyamotoi infection leads to cross-reactive antibodies to the C6 peptide in mice and men. Clin Microbiol Infect, 2019;26:513.e1–513.e6.

167. Hulínská D, Kybicová K. Diagnostika lymeské borreliózy v NRL LB [online] 2008-05-14 [cit. 2020-01-26]. Dostupné na www: http:// www.szu.cz/tema/prevence/diagnostika-lymeske-borreliozy-v- -nrl-lb.

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