Паразитарная система Ixodes persulcatus (Ixodinae) – Borrelia garinii – мелкие млекопитающие на северо-западе России

Л.А. Григорьева, O.A. Mитева и E.П. Самойлова

Труды Зоологического института РАН, 2024, 328(2): 308–322   ·   https://doi.org/10.31610/trudyzin/2024.328.2.308

Полный текст  

Резюме

Исследованы взаимоотношения между членами паразитарной системы, образуемой таёжным клещем Ixodes persulcatus (Schulze, 1930) на преимагинальных фазах развития, Borrelia garinii и мелкими млекопитающими. Установлено, что трансовариальная передача B. garinii у таежного клеща отсутствует. В условиях природных биотопов северо-запада России мелкими млекопитающими, прокормителями преимагинальных стадий Ixodes persulcatus являются Myodes glareolus (Schreber, 1780) (52–53%), Sorex araneus Linnaeus, 1758 (33–34%), Apodemus uralensis (Pallas, 1811) (14%). Личинки и нимфы наиболее многочисленны на прокормителях в начале сезона, в мае и июне. В дальнейшем их численность снижается в 5–10 раз и может немного увеличиваться в сентябре. В популяциях до 31.9 % особей M. glareolus и 20.5% особей A. uralensis инфицированы B. garinii. Установлен агрегированный тип распределения личинок и нимф таёжного клеща на прокормителях. Инфицирование основной части голодных личинок и нимф происходит в начале сезона активности после зимовки при питании на перезимовавших инфицированных прокормителях. Этот период является ключевым в циркуляции (обмене между переносчиками и резервуарными хозяевами) и сохранении B. garinii в природном очаге боррелиоза на северо-западе России. Вертикальная передача B. garinii возможна от напитавшихся в начале сезона личинок и нимф перелинявшим в августе-сентябре нимфам и взрослым клещам, соответственно. Горизонтальная передача возбудителя от мелких млекопитающих, особенно рыжей полевки, личинкам и нимфам и наоборот обеспечивает циркуляцию и сохранение B. garinii в природных очагах. Вопрос о сохранении возбудителя в зимующих преимагинальных стадиях клещей требует дальнейших исследований.

Ключевые слова

Borrelia garinii, Ixodes persulcatus, мелкие млекопитающие

Поступила в редакцию 20 мая 2023 г.  ·  Принята в печать 11 апреля 2024 г.  ·  Опубликована 24 июня 2024 г.

Литература

Balashov Y.S. 2009. Acari and Insect Parasitism on Terrestrial Vertebrates. Nauka, Saint Petersburg, 357 p. [In Russian].

Balashov Yu.S., Bochkov A.V., Vaschenok V.S., Grigorieva L.A., Stanjukovich M.K. and Tretjakov K.A. 2007. Structure of populations and ecological nishes of ectoparasites in the parasite communities of small forest mammals. Parasitologiya, 41(5): 329–347. [In Russian].

Babenko L.V. 1985. Seasonal variations of activity. In: N.A. Filippova (Ed.) Taiga tick Ixodes persulcatus Schulze (Acarina, Ixodidae): morphology, systematics, ecology. Nauka, Leningrad: 220–230. [In Russian].

Beklemishev V.N. 1970. Terms and concepts necessary for the quantitative study of populations of ectoparasites and nidicols. In: V.N. Beklemishev. Biocenological foundations of comparative parasitology. Nauka, Moscow: 143–154. [In Russian].

Bobretsov A.V. 2016. Population ecology of small mammals of plains and mountain landscapes of the north-east of the European part of Russia. Association of scientific publications KMK, Moscow, 381 p. [In Russian].

Coipan C., Fonville M., Tijsse-Klasen E., Van der Giessen J.W.B., Takken W., Sprong H. and Takumi K. 2013. Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S–23S rDNA spacer region. Infection, Genetics and Evolution, 17: 216–222. https://doi.org/10.1016/j.meegid.2013.04.009

Filippova N.A. 1977. Ixodid ticks subfamily Ixodinae (Fauna USSR). Arachnida, 4(4): 272–283, 316–330. [In Russian].

Filippova N.A. 1990. Taxonomic Aspects of Transmission of the Lyme Disease Pathogen. Parazitologiya, 24(4): 257–267. [In Russian].

Gern L. 2009. Life Cycle of Borrelia burgdorferi sensu lato and Transmission to Humans. Current Problems in Dermatology, 37: 18–30. https://doi.org/10.1159/000213068

Gern L. and Rais O. 1996. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology, 33: 189–192. https://doi.org/10.1093/jmedent/33.1.189

Gorelova N.B., Korenberg E.I., Kovalevskii Yu.V., Postic D. and Baranton G. 1996. Isolation of borrelia from the tick Ixodes trianguliceps (Ixodidae) and the significance of this species in epizootiology of ixodid tick-borne borrelioses. Parasitologiya, 30(1): 13–18. [In Russian].

Gorelova N.B., Korenberg E.I., Kovalevskii Yu.V. and Shcherbakov S.V. 1995. Small mammals as reservoir hosts for Borrelia in Russia. Zentralblatt für Bakteriologie, 282: 315–322. https://doi.org/10.1016/S0934-8840(11)80132-5

Grigoryeva L.A. 1996. A common shrew as a reservoir of borrellae in the north-west of Russia. Parasitologiya, 30(5): 470–72. [In Russian].

Grigoryeva L.A. and Miteva O.A. 2022. Transovarial and transphase transmission by the ship tick Ixodes ricinus of the causative agent of Ixodes tick-borne borreliosis Borrelia valaisiana. Reporting scientific session of ZIN RAS based on the results of work in 2020–2021. Abstracts. May 17–19, Saint Petersburg: 17–18. [In Russian].

Grigoryeva L.A. and Stanyukovich M.K. 2016. Life cycle of the taiga tick Ixodes persulcatus (Acari: Ixodidae) in the North-West of Russia. Experimental and Applied Acarology, 69: 347–357. https://doi.org/10.1007/s10493-016-0038-1

Grigoryeva L.A. and Stanyukovich M.K. 2018. Differential diagnosis of Ixodes ricinus and Ixodes persulcatus: nymphs and larvae. Experimental and Applied Acarology, 75(1): 97–106. https://doi.org/10.1007/s10493-018-0244-0

Grigoryeva L.A. and Tretyakov K.A. 1998. Peculiarity of parasitic system ixodid ticks – borrelia – micromammalia in the north-west of Russia. Parasitologiya, 32: 422–430. [In Russian].

Grigoryeva L.A., Miteva O.A., Myasnikov V.A., Gogolevsky A.S. and Shitova L.F. 2019. The effect of infection of hard ticks Ixodes ricinus (L.) and Ixodes persulcatus Sch. (Acari: Ixodinae) with the causative agent of Lyme borreliosis (Borrelia burgdorferi s. l.) on their host search activity (using attractants). Systematic and Applied Acarology, 24(12): 2358–2368. https://doi.org/10.11158/saa.24.12.6

Humair P.F., Peter O., Wallich R. and Gern L. 1995. Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. Journal of Medical Entomology, 32(4): 433–438. https://doi.org/10.1093/jmedent/32.4.433

Korenberg E.I., Gorelova N.B. and Kovalevskii Y.V. 2002. Ecology of Borrelia burgdorferi sensu lato in Russia. In: J.S. Gray, O. Kalh, R.S. Lane and G. Stanek (Eds). Lyme borreliosis. Biology, Epidemiology and Control. New York, CABI Publishing: 175–200. https://doi.org/10.1079/9780851996325.0175

Korenberg E.I., Gorban L.Y., Kovalevskii Y.V., Frisen V.I. and Karavanov A.S. 2001. Risk for human tick-borne encephalitis, borreliosis, and double infection in the pre-Ural region of Russia. Emerging Infectious Diseases, 7: 459–462. https://doi.org/10.3201/eid0703.017319

Korenberg E. and Likhacheva T. 2006. Analysis of the long-term dynamics of tick-borne encephalitis (TBE) and ixodid tick-borne borrelioses (ITBB) morbidity in Russia. International Journal of Medical Microbiology, 296(Suppl. 1): 54–58. https://doi.org/10.1016/j.ijmm.2006.02.001

Korenberg E.I., Pomelova V. and Osin N. 2013. Infections with natural focality transmitted by ixodid ticks. Moscow, 463 p. [In Russian].

Korenberg E.I., Sirotkin M.B. and Kovalevskii Y.V. 2016. A general scheme of circulation of Ixodid Tick-Borne Borrelioses Pathogens in the Natural Foci of Eurasia. Entomolological Review, 96: 484–499. https://doi.org/10.1134/s0013873816040126

Korotkov Yu.S., Kislenko G.S., Burenkova L.A., Rudnikova N.A. and Karan L.S. 2008. Spatial and temporal variability of Ixodes ricinus and Ixodes persulcatus infection with the Lyme disease agent in Moscow region. Parasitologiya, 6: 441–451.

Kurtenbach K., De Michelis S., Sewell H.S., Etti S., Schafer S.M. and Holmes E. 2002. The key roles of selection and migration in the ecology of Lyme borreliosis. International Journal of Medical Microbiology, 291(Suppl. 33): 152–154. https://doi.org/10.1016/S1438-4221(02)80029-7

Kurtenbach K., Sewell H.S., Ogden N.H., Randolph S.E. and Nuttall P.A. 1998. Serum complement sensitivity as a key factor in Lyme disease ecology. Infection and Immunity, 66: 1248–1251. https://doi.org/10.1128/IAI.66.3.1248-1251.1998

Margos G., Vollmer S.A., Ogden N.H. and Fish D. 2011. Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infection, Genetics and Evolution, 11: 1545–63. https://doi.org/10.1016/j.meegid.2011.07.022

Mongodin E.F., Casjens S.R., Bruno J.F., Xu Y. et al. 2013. Inter- and intra-specific pan-genomes of Borrelia burgdorferi sensu lato: genome stability and adaptive radiation. BMC Genomics, 14: 693. https://doi.org/10.1186/1471-2164-14-693

Naumov R.L., Vasilieva I.S., Gutova V.P. and Ershova A.S. 1998. Reproduction of the Lyme disease spirochete Borrelia burgdorferi s. l. in the taiga tick Ixodes persulcatus. Parasitologiya, 32(5): 412–421. [In Russian].

Nefedova V.V., Korenberg E.I. and Gorelova N.B. 2010. Genetic variants of Borrelia garnii, a widespread Eurasian causative agent of diseases of ixodic tick borreliosis. Molecular Genetics, Microbioljgy and Virology, 25: 95–100. [In Russian] https://doi.org/10.3103/s089141681003002x

Ogden N.H., Artsob H., Margos G. and Tsao J. 2014. Non-rickettsial tick-borne bacteria and the diseases they cause. In: Sonenshine, DE, Roe, RM (Eds), Biology of ticks. Vol. 2, Oxford University Press: 278–312.

Postic D., Assous M.V., Grimont P.A.D. and Baranton G. 1994. Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. International Journal of Systematic Bacteriology, 44: 743–752. https://doi.org/10.1099/00207713-44-4-743

Postic D., Korenberg E., Gorelov N., Kovalevskii Yu.V., Belenger E. and Baranton G. 1997. Borrelia burgdorferi sensu lato in Russia and neighbouring countries: high incidence of mixed isolates. Research in Microbiology, 148: 691–702. https://doi.org/10.1016/s0923-2508(99)80068-0

Pritt B.S., Mead P.S., Johnson D.K.H., Neitzel D.F. et al. 2016. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: A descriptive study. Lancet Infection Diseases, 16: 556–564. https://doi.org/10.1016/s1473-3099(15)00464-8

Rudenko N., Golovchenko M., Vancova M., Clark K., Grubhoffer L. and Oliver J.H. 2016. Isolation of live Borrelia burgdorferi sensu lato spirochaetes from patients with undefined disorders and symptoms not typical for lyme borreliosis. Clinical Microbiology and Infection, 22: 267. https://doi.org/10.1016/j.cmi.2015.11.009

Scott J.D., Foley J.E., Anderson J.F., Clark K.L. and Durden L.A. 2017. Detection of Lyme disease bacterium, Borrelia burgdorferi sensu lato, in blacklegged ticks collected in the Grand River Valley, Ontario, Canada. International Journal of Medical Sciences, 14: 150. https://doi.org/10.7150/ijms.17763

Skuballa J., Oehme R., Hartelt K., Petney T., Bücher T., Kimmig P. and Taraschewski H. 2007. European hedgehogs as hosts for Borrelia spp. in Germany. Emerging Infectious Diseases, 13(6): 952–953. https://doi.org/10.3201/eid1306.070224

Tsao J.I. 2009. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Veterinary Research, 40: 36. https://doi.org/10.1051/vetres/2009019

Tupikova N.V. and Kaleda L.V. 1957. Determining the age of rodents. In: A.N. Formozov (Ed.). Fauna and ecology of rodents. Moscow University Press, 5: 119–154. [In Russian].

Vasilieva I.S. and Naumov R.L. 1996. Lyme disease-parasitosis system, the state of the problem communication. I. Pathogens and vectors. Acarina, 4: 53–75. [In Russian].

Vennestrøm J., Egholm H. and Jensen P.M. 2008. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. International Parasitology, 57: 32–37. https://doi.org/10.1016/j.parint.2007.07.004

Wang G. 2015. Chapter 104 – Borrelia burgdorferi and other Borrelia species. In: Y.-W. Tang, D. Liu, J. Schwartzman, M. Sussman and I. Poxton (Eds). Molecular Medical Microbiology, 3: 1867–1909. https://doi.org/10.1016/b978-0-12-397169-2.00104-9

 

© Зоологический институт Российской академии наук
Последнее изменение: 23 сентября 2024 г.