The first cases of Borrelia miyamotoi disease in the Far East of Russia


Leonova G.N., Bondarenko E.I., Ivanis V.A., Belikov S.I., Lubova V.A.

1G.P. Somov Research Institute of Epidemiology and Microbiology, Vladivostok, Russia; 2«Vector-Best», Novosibirsk, Russia; 3Pacific State Medical University, Vladivostok, Russia; 4Limnological Institute, Siberian Branch, Russian Academy of Sciences, Irkutsk, Russia
Investigations were conducted to identify tick-borne pathogens, including tick-borne encephalitis virus, Borrelia, Anaplasma, Ehrlichia, in the south of the Russian Far East.
Objective. To verify Borrelia miyamotoi in Ixodes ticks and in the blood of patients and to describe cases.
Materials and methods. In 2014–2015, the investigators studied 238 I. persulcatus samples collected from vegetation; 253 I. persulcatus samples taken from patients; and 168 leukocyte fraction samples from patients after tick suction. Real-time PCR was performed using MultiPrime reagent kits for the amplification of cDNA fragments of tick-borne encephalitis virus, B. burgdorferi s.I, A. phagocytophilum, E. chaffeensis/E. muris-FL (Central Research Institute of Epidemiology, Moscow), and B. miyamotoi («Vector-Best», Novosibirsk). The B. miyamotoi glpQ regions with a length of 680 bp were sequenced.
Results. The typical symptoms of the disease caused by B. miyamotoi were detected in only two out of 21 verified patients (14 I. persulcatus specimens taken from the patients and 7 leukocyte fraction samples from the patients after tick suction). Sequencing of the glpQ gene and phylogenetic analysis showed genetic differences between B. miyamotoi and B. burgdorferi s.I. and a similarity with the pathogens of a relapsing fever Borrelia group.
Conclusion. Among the tick-borne pathogens, not only B. burgdorferi s.l. causing Lyme disease, but also the new pathogen B. miyamotoi previously unknown in the Far East plays a great role.

Literature


1. Sarksian D.S., Platonov A.E., Karan L.S., Malinin I.E., Halitova L.I., Shahov V.I., Dudarev M.V., Malinin O.V., Maleev V.V. [Clinical features of the «new» borreliosis caused by Borrelia miyamotoi]. Terapevticheskij arkhiv 2012; 84(11): 34–41. (In Russ.).

2. Bagautdinova L.I., Sarksian D.S., Dudarev M.V., Malinin O.V., Kustarnikov G.K., Shakhov V.I. [Clinical polymorphism of the disease caused by Borrelia miyamotoi]. Prakticheskaja meditcina 2013; 5(74): 125–30. (In Russ.).

3. Fukunaga M., Takahashi Y., Tsuruta Y., Matsushita O., Ralph D., Mcclelland M., Nakao M. 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: 804–10.

4. Bondarenko E.I., Sibirtceva G.S., Tkachev V.K., Viatkina T.G., Baranova S.G., Timofeev D.I., Ivanov M.K. [Differential approach to the identification of Borrelia in ticks and clinical samples by PCR analysis in real-time using a set of the series «Real-Best»]. VIII Vserossiyskaya nauchno-prakticheskaya konferentsiya s mezhdunarodnym uchastiem «Molekulyarnaya diagnostika – 2014». Mosсоw, 2014; 1: 503–4. (In Russ.).

5. Platonov A.E., Karan L.S., Garanina S.B., Shopenskaya T. A., Kolyasnikova N.M., Platonova O.V., Fedorova M.V. [Natural focal infections in the XXI century in Russia]. Еpidemiologiуa i Infekcionnye Bolezni 2009; (2): 38–44. (In Russ.).

6. Hovius J.W., de Wever B., Sohne M., Brouwer M.C., Coumou J., Wagemakers A. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 2013; 382: 658. DOI:10.1016/S0140-6736(13) 61644-X.

7. Molloy P.J., Telford S.R. III, Chowdri H.R., Lepore T.J., Gugliotta J.L., Weeks K.E., Hewins M.E., Goethert H.K., Berardi V.P. Borrelia miyamotoi disease in the Northeastern United States: a case series. Ann. Intern. Med. 2015; 163(2):91–8. DOI:10.7326/M15-0333

8. Karan L.S., Koliasnikova N.M., Makhneva N.A., Toporkova M.G., Nadezhdina M.V., Esaulkova A.Yu., Romanenko V.V., Arumova E.A., Platonov A.E., Maleev V.V. [Application of PCR in real time for the diagnosis of tick-borne infections caused by tick-borne encephalitis virus, B. burgdorferi s. l, B. miyamotoi, A. phagocytophillum, E. muris, E. chaffeensis]. Zhurnal Mikrobiologii, Epidemiologii i Immunobiologii 2010; (3): 72–7. (In Russ.).

9. Karan L.S., Koliasnikova N.M., Sarksian D.S., Gridneva K.A., Fedorova M.V., Esaulkova A.U., Romanenko V.V. [Infection ixodes ticks and small mammals, borrelia different taxonomic groups]. Molekuliarnaуa diagnostika 2014; (1): 493–4 (In Russ.).

10. Bondarenko E.I., Pozdnyakov L.L., Sibirtseva G.S., Timofeyev D.I., Fomenko N.V., Ivanov M.K. [Reagent kit for the detection of Borrelia miyamotoi – the causative agent of tick-borne relapsing fever by PCR in real-time]. Novosti «Vektor-Best» 2013; 1(67): 2–19. (In Russ.).

11. Rar V.A., Epikhina T.I., Tikunova N.V., Bondarenko E I., Ivanov M.K., Yakimenko V.V., Malkova M.G., Tancev A.K. [DNA detection of pathogens transmitted by ixodid ticks in blood of small mammals inhabiting the forest biotopes in middle Irtysh area (Omsk region, West Siberia) ]. Parasitologiya 2014; 48(1): 37–53. (In Russ.).

12. Leonova G.N., Bondarenko E.I., Khvorostianko A.A., Kurlovskaia A.V. [The study of the prevalence in the south of the Far East pathogens transmitted by Ixodes ticks]. Epidemiologiуa i Vaktcinoprofilaktika 2015; (1): 31–5. (In Russ.).

13. Platonov A.E., Karan L.S., Kolyasnikova N.M., Makhneva N.A., Toporkova M.G., Maleev V.V., Fish D., Krause P.J. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg. Infect. Dis. 2011; 17: 1816–23.: DOI: 10.3201/eid1710.101474.

14. Gugliotta J.L., Goethert H.K., Berardi V.P., Telford S.R. III. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N. Engl. J. Med. 2013; 368: 240–245. http://dx.doi.org/10.1056/NEJMoa1209039

15. Krause P.J., Narasimhan S., Wormser G.P., Rollend L., Fikrig E., Lepore T. Human Borrelia miyamotoi infection in the United States. N. Engl. J. Med. 2013; 368: 291–3. DOI: 10.1056/NEJMc1215469.

16. Chowdri H.R., Gugliotta J.L., Berardi V.P., Goethert H.K., Molloy P.J., Sterling S.L., Telford S.R. Borrelia miyamotoi infection presenting as human granulocytic anaplasmosis: a case report. Ann. Intern. Med. 2013; 159: 21–7. DOI: 10.7326/0003-4819-159-1-201307020-00005

17. Sato K., Takano A., Konnai S., Nakao M., Ito T., Koyama K., Kaneko M., Ohnishi M., Kawabata H. Human infections with Borrelia miyamotoi, Japan. Emerg. Infect. Dis. 2014; 20(8): 1391–3. DOI: 10.3201/eid2008.131761.

18. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007; 24(8): 1596–9.

19. Barbour A.G., Bunikis J., Travinsky B., Hoen A.G., Diuk- Wasser M.A., Fish D., Tsao J.I. 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. DOI: 10.4269/ajtmh.2009.09-0208

20. Krause P. J., Fish D., Narasimhan S., Barbour A. G. Borrelia miyamotoi infection in nature and in humans. Clin. Microbiol. Infect. 2015; 21(7): 631–9.

21. Sarksyan D.S. [Ixodes tick-borne borreliosis – state of the problem]. Infektsionnye bolezni 2015; (2): 61–7. (In Russ.).

22. Krause P.J., Hendrickson J.E., Sleeves T.K., Fish D. Blood transfusion transmission of the tick-borne relapsing fever spirochete Borrelia miyamotoi in mice. Transfusion 2015. http://dx.doi.org/10.1111/trf.12879 [Epub ahead of print].

23. Platonov A.E., Koetsveld J., Sarksyan D.S., Platonova O.V., Semenova M.V., Tetelyutina F.K., Maleev V.V. [Pregnancy and childbirth pathology in tick-borne relapsing fever]. Èpidemiologiâ i infekcionnye bolezni. Аktual'nye voprosy 2015; (6): 34–45. (In Russ.).


About the Autors


For correspondence:
Prof. Galina N. Leonova, MD, Principal Researcher, G.P. Somov Research Institute of Epidemiology and Microbiology
Address: 1 Selskaya St., Vladivostok 690087, Russia
Telephon: +7(423) 244-07-12
E-mail: galinaleon41@gmail.com
Information about the authors:
Еvgeni I. Bondarenko, Cand. Biol. Sci., Researcher, AO «Vector-Best», Novosibirsk, Russia; е-mail: ebondarenko@ngs.ru
Viktoria A. Ivanis, MD, Professor, Department of Infectious Diseases, Pacific State Medical University, Vladivostok, Russia; е-mail: ivanis2003@bk.ru
Prof. Sergei I. Belikov, BD, Head of Laboratory, Limnological Institute, Siberian Branchof the Russian Academy of Sciences, Irkutsk, Russia; e-mail: sergeibelikov47@gmail.com
Viktoria A. Lubova, Junior Researcher, G.P. Somov Research Institute of Epidemiology and Microbiology, Vladivostok, Russia; e-mail: valeri_priority@mail.ru


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