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ИНФЕКЦИОННЫЕ БОЛЕЗНИ INFECTIOUS DISEASES
DOI: 10.29413/ABS.2018-3.2.6 УДК 616-036.22; 616-07:061.62
Khasnatinov M.A. Rychkova L.V. Rodriguez I. 2, Corona B. 3, Danchinova G.A. 1
IXODID TICKS AND TICK-BORNE INFECTIONS IN THE REPUBLIC OF CUBA -LITERATURE REVIEW AND RATIONALE FOR RISK ASSESSMENT
1 Scientific Centre for Family Health and Human Reproduction Problems (ul. Timiryazeva 16, Irkutsk 664003, Russian Federation) 2 Institute of Tropical Medicine Pedro Kouri (P.O.B. 601, Marianao 13, Habana, Cuba)
3 National Centre for Animal and Plant Health (Apartado 10, 32700, San José de las Lajas, La Habana, Cuba)
The Republic of Cuba is a popular destination for Russian tourists and about 30-50 thousands of Russian citizens visit Cuba annually. However, the recreational activity is often associated with the risk of Ixodid ticks bites and infection with tick-borne pathogens. According to published literature, the fauna of the hard tick in Cuba is represented by nine species including Ixodes capromydis, Amblyomma albopictum, A. cajennense, A. dissimile, A. quadricavum, A. torrei, Dermacentor nitens, Rhipicephalus sanguineus and R. (Boophilus) microplus. Five of these species, i.e. A. cajennense, A. dissimile, D. nitens, R. sanguineus and R. (Boophilus) microplus, were reported as human parasites. Ticks are spread over the most part of the island territory. Several tick-borne pathogens should be considered as a potential threat for the bitten humans in Cuba, including Borrelia burgdorferi sensu lato, Rickettsia sp., Anaplasma sp., Ehrlichia sp., Coxiella sp., thogotovirus and Crimean-Congo hemorrhagic fever virus. Implications for the epidemiology of tick-borne infections in the Russian Federation are discussed. Key words: ticks, Ixodidae, Cuba, Russia, tick-borne infections
ИКСОДОВЫЕ КЛЕЩИ И ПЕРЕДАВАЕМЫЕ ИНФЕКЦИИ В РЕСПУБЛИКЕ КУБА -ОБЗОР ЛИТЕРАТУРЫ И ОБОСНОВАНИЕ ДЛЯ ОЦЕНКИ РИСКА ЗАРАЖЕНИЯ
Хаснатинов M.A. Рычкова Л.В. Родригес И. 2, Корона Б. 3, Данчинова Г.А. 1
1ФГБНУ «Научный центр проблем здоровья семьи и репродукции человека»
(664003, г. Иркутск, ул. Тимирязева, 16, Россия)
2 Институт тропической медицины имени Педро Коури
(г. Гавана, Марианао 13, а/я 601, Республика Куба)
3 Национальный центр здоровья животных и растений (32700, Гавана, Сан-Хосе-де-лас-Лахас, а/я 10, Республика Куба)
С каждым годом растёт привлекательность Республики Куба в качестве места отдыха граждан Российской Федерации. Ежегодно эту страну посещают с туристическими целями порядка 30-50 тысяч наших соотечественников. Однако отдых на природе зачастую связан срискомукусов иксодовых клещей и заражения передаваемыми ими инфекциями. Согласно опубликованным к настоящему моменту данным, на территории Кубы обитают девять видов иксодовых клещей, включая Ixodes capromydis, Amblyomma albopictum, A. cajennense, A. dissimile, A. quadricavum, A. torrei, Dermacentor nitens, Rhipicephalus sanguineus и R. (Boophilus) microplus. Пять из этих видов, а именно A. cajennense, A. dissimile, D. nitens, R. sanguineus и R. (Boophilus) microplus, были отмечены в качестве паразитов человека. Клещи распространены на большей части территории острова. Несколько патогенов, передающихся приукусах клещей, следует рассматривать в качестве возможнойугрозы для здоровья людей, пострадавших от укуса клеща на Кубе. Это, прежде всего, Borrelia burgdorferi sensu lato, Rickettsia sp., Anaplasma sp., Ehrlichia sp., Coxiella sp., вирус Тогото и вирус Крымской-Конго геморрагической лихорадки. В работе обсуждаются возможные последствия для эпидемиологии клещевых инфекций в Российской Федерации.
Ключевые слова: иксодовые клещи, Ixodidae, Куба, Россия, клещевые инфекции
In the modern world, the international journeys are a significant part of the global economy. Millions of people travel worldwide annually. In recent years, it became usual for tourists from the Russian Federation to travel to remote countries with a warm tropical and subtropical climate. However, the recreational activity is often associated with a risk of infection with
vector-borne pathogens. Ixodid ticks that are very important disease vectors can bite both locals and travelers. Thus, according to our observations, up to 10 residents of the Irkutsk Region get a tick bite while traveling abroad annually. Tick bites were reported in 18 countries including such remote ones as Thailand, Japan, United Kingdom and USA [6].
The Republic of Cuba is included in the top 50 countries that are visited by tourists from the Russian Federation. Thus, according to the Federal Agency for Tourism of Russian Federation (Russiatourism), 44 951 Russian citizens visited Cuba in 2016. The annual increase of tourist exchange between Cuba and Russia over last 3 years reached 129 % [32]. Recently, a case of tick bite was reported by a Russian tourist while visiting historical site suburbs of Havana (L.V. Rychkova, personal communication).
The aim of this review is to summarize briefly the published information about the fauna of ixodid ticks in the Republic of Cuba and evaluate its implications for epidemiology of tick-borne diseases in Russia. The publications were selected from the PubMed database (https:// www.ncbi.nlm.nih.gov/pubmed) using key phrases "tick+Cuba", "Ixod+Cuba", "Dermacentor+Cuba", "Haema-physalis+Cuba", "Amblyomma+Cuba", "Tick-borne+Cuba", "Borrelia+Cuba", and "Anaplasm+cuba". The results were manually filtered according to the relevance. Taxonomy of Ixodidae family is used according to Filippova, 1997 [12].
FAUNA AND DISTRIBUTION OF TICKS IN CUBA
The fauna of the hard tick in Cuba is represented by nine species belonging to genera Ixodes, Amblyomma, Dermacentor and Rhipicephalus. The only representative of Ixodinae subfamily is the Cuban endemic Ixodes capro-mydis. The subfamily Amblyomminae is presented by five Amblyomma (A. albopictum, A. cajennense, A. dissimile, A. quadricavum, A torrei), one Dermacentor (D. nitens), and two Rhipicephalus species (R. sanguineus and R. (Booph-ilus) microplus) [2].
A. albopictum Neumann, 1899 is associated with reptiles (snakes and lizards) as primary hosts. These ticks are spread over the Central America and inhabit tropical and subtropical dry broadleaf forests, deserts and xeric shrublands [17]. In Cuba, these ticks were detected in the Province of La Havana, Camaguey, Doce Leguas Cayos, Isle of Pines, and Isla De La Juventud [2, 36]. The ecology of these highly specialized ticks is not so far described completely, and no attacks on humans reported for A. albopictum.
A. cajennense (Fabricius, 1787) is widespread over Nearctic and Neotropical regions from the United States on the North to Argentina on the South. This tick has adapted to widely different ecological conditions, including ecosystems as different as semi-arid grasslands and subtropical secondary forests. A. cajennense prefers mild tropical climate with the mean annual temperature above 16-17 °C and does not appear to have been collected north of 27° N or south of 29° S [10]. In Cuba, it has been reported in Provinces of Havana, Pinar del Rio, and Villa Clara [36] as well as from Provinces of Santiago de Cuba, Camaguey, and Isla De La Juventud [2]. These ticks parasitize over a broad range of mammalian and avian hosts, with reptiles and anura reported as exceptional hosts. Several species of birds belonging to orders Ciconiiformes, Falconiformes, Struthioniformes, Cuculi-formes, Galliformes, Passeriformes and Columbiformes were reported as hosts for A. cajanense [17]. Adult ticks feed on equids, cattle, dogs, wild carvivores (Canidae and Procionidae) and ungulates (Tapiridae, Tayassuidae and Cervidae). Immature stages feed on numerous rodent species, wild carnivores and ungulates [10]. A. cajanense
is a frequent parasite of humans in Neotropical regions. Numerous human bites are reported from such countries as Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Suriname and Venezuela [15].
A. dissimile Koch, 1844 is widespread over the Neotropical and Neoarctis and inhabits tropical and subtropical dry broadleaf forests, grasslands, savannas and shrublands [17]. Primary hosts for A. dissimile are Squa-mata (63 species) and Anura (4 species). Mammals, birds and crocodiles are exceptional hosts [16]. The transport of A. dissimile to the boreal ecosystems of Canada with migrating passerine birds (veery, Catharus fuscescens) has been recently documented [34]. These ticks are well known parasites of humans [15, 16].
A. quadricavum (Schulze, 1941) is a Neotropical tick inhabiting tropical and subtropical moist broadleaf forests. Usual hosts for these ticks are boas, iguanas and vipers [17]. Curiously, five specimens ofA. quadricavum were accidentally introduced into Poland with pet lizards (Iguana iguana) imported from El Salvador [27]. No cases of human infestation have been registered for A. quadricavum so far.
A. torrei Perez Vigueras, 1934 are parasites of Squa-mata (lizards and iguanas mostly). The Anura may serve as exceptional hosts for A. torrei. These ticks inhabit tropical and subtropical moist broadleaf forests and mangroves and distributed in provinces of Camaguey, La Habana, Playa De Jaimanitas, Guanahacabibes, and Pinar Del Rio [2, 36]. No human infestation has been reported.
D. nitens Neumann, 1897, or tropical horse tick, is widespread in neotropical ecosystems. It is widely distributed over the entire island and it has been reported in Provinces of Havana, Pinar del Rio, Santa Clara, Matanzas, and Camaguey [36]. D. nitens is one-host ticks with equines serving as the primary host. However, many other domestic and wild animals, including bovines, ovines, felines and rabbits, can serve as alternative hosts [discussed in: 29]. Snakes and toads are also reported as exceptional hosts for D. nitens [17]. A number of cases of D. nitens feeding on human host were registered in Bolivia, Brazil and Colombia [15].
I. capromydis Cerny, 1966 is Cuban endemic and reported only from Guayacanal (Juventud Island, Cuba). Main habitation for this ticks are Cuban pine forests [3]. I. capromidesis associated with a specific mammalian host Capromys pilorides (Rodentia: Capromyidae) or Cuban hutia. These large rodents are widely distributed not only on the Juventud Island, but also on the Cuban mainland and many other islands of the Cuban archipelago [38]. The populations of hutia are numerous and the density may reach 50 animals per hectare [1]. Cuban hutia is reported to be the object of hunting and keeping in captivity as a livestock [28]. There have been no reports of feeding of I. capromydis on humans so far.
R. microplus (Canestrini, 1887) is a cosmopolitan species inhabiting many ecoregions in tropical and sub-tropical areas worldwide. Bovidae serve as main hosts for R. microplus, whereas birds and reptiles are registered as exceptional hosts [17]. In Cuba, these ticks are spread in the provinces of San Juan y Martinez, Santiago De Las Vegas, Pinar Del Rio, Bayamo, Guane, Isla De La Juventud, and Santiago De Cuba [2]. Numerous cases of human infestation are documented in many countries of South America [15].
R. sanguineus (Latreille, 1806) inhabits both Old and New Worlds. In Cuba, the species has been found in the provinces of La Habana, Camagüe, San Juan y Martínez, Isle of Pines, Santiago de Las Vegas, and Pinar del Rio [2]. These ticks are considered as a group of closely related groups with yet unresolved taxonomic status and are proposed to be designated as R. sanguineus sensu lato [8]. Ticks identified as R. sanguineus s.l. were exclusively found on dogs, however occasionally, R. sanguineus can infest a wide range of domestic and wild hosts, including cats, rodents and birds. [7, 8]. R. sanguineus is a recognized parasite biting humans both at imago and nymphal stages and is able to infest densely populated urban areas [15, 35]
TICK-BORNE INFECTIONS
To date, several tick-borne infections of humans and domestic animals were shown to circulate in the Cuban ecosystems. The agents of human granulocytic anaplasmo-sis (HGA), Anaplasma spp., were detected in R. sanguineus [31]. Besides this, the antibodies against Lyme disease (LD) agent Borrelia burgdorferi sensu lato [30], Babesia bovis and B. bigemina [35] were detected in the blood of the local residents. The Anaplasma marginale that is a significant cattle pathogen was isolated both in western and in eastern parts of the country [4]. Authors emphasize that ixodid ticks pose the serious threat for human health and stock rising in developing countries [31]. Recently, it has been shown that D. nitens ticks can harbour the Borrelia burgdorferi sensu stricto [13], that suggest the vector capacity of these ticks for Lyme disease in Cuba. A. cajanense was demonstrated as a biological vector for Theileria (Babesia) equi - an important haemoparasite of equines [33]. R. sanguineus have been regarded as a vector for a number of pathogenic microorganisms, including significant human pathogens such as Crimean-Congo hemorrhagic fever virus (CCHFV), Thogotovirus Thog-oto (THOV), Coxiella burnetii (agent of Q-fever), E. canis, E. chaffeensis, R. conorii (agent of Mediterranean spotted fever), R. massiliae (agent of spotted-fever) and R. rick-ettsii (agent of Rocky Mountain spotted fever) [7, 19, 20]. R. microplus can transmit the Babesia spp. and Anaplasma marginale, agents that can cause a severe disease in cattle and often have major impacts on livestock production [2].
IMPLICATIONS FOR EPIDEMIOLOGY OF TICK-BORNE INFECTIONS IN RUSSIA
The official registration indicates about 15 000 reported tick bites annually in the Irkutsk region. There are six species of ixodid ticks inhabiting the Pribaikalye region - Ixodespersulcatus Schulze, 1930; I. lividus Koch, 1844; I. trianguliceps Birula, 1895; Dermacentor nuttalli Olenev, 1929; D. silvarum Olenev, 1932 and Haemaphys-alis concinna Koch, 1844. Besides this the rare occasional findings of I. subterraneus Filippova, 1961, I. crenulatus Koch, 1844, I. berlesei Birula, 1895, u I. stromi Filippova, 1957 were reported from the Eastern Siberia and neighbor territories [5, 11, 23, 24, 25]. To reduce the risk of human infection, the technology of urgent detection and prevention of tick-borne diseases was developed and implemented at the Federal Budgetary Scientific Center for Family Health and Human Reproduction Problems (FBSC FHHRP) in Irkutsk. Each tick is routinely tested for
infection with TBEV, B. burgdorferi sensu lato, A. phago-cytophilum and E. muris/E. chaffeensis. In case when any pathogen is detected in the tick, the patient receives the treatment with anti-TBEV immunoglobulins and/or antibiotics to prevent the disease according to modern Russian healthcare regulations. However, the analyzed literature data indicate that people bitten by the Cuban ticks can be infected with other pathogens, those will be not detected by the currently used tests. Thus, in case when residents of Russia report a tick bite while being in Cuba, the infection with Rickettsia sp., Anaplasma sp., Coxiella sp., THOV, CCHFV should be considered as possible in addition to usual tick-borne pathogens.
Besides this, during the last decade several people were attacked by ticks that are exotic for the Eastern Siberia. In 2008, we revealed the unique case of sucking of Amblyomma americanum in the suburban area of Irkutsk city. Epidemiological investigation excluded the import of tick from abroad either by the bitten patient or by domestic pets. It was revealed that the causative tick was indeed molted and questing in the Siberian ecosystem [22, 26]. In 2013 and 2014, there were local cases of tick bites caused by Rhipicephalussanguineus Latreille, 1806. The detailed study confirmed the local origin of all these exotic ticks and revealed the existence of at least three independent migration routes of A. americanum and R. sanguineus into the Eastern Siberia from genetically divergent populations. All these ticks were able to migrate several thousands kilometers from their convenient ecosystems and survive at least for some time in continental climate [22]. It can not be excluded that exotic ticks may migrate from Cuba as well and any inconvenient tick need to be carefully studied to identify its species.
CONCLUSION
Published data clearly demonstrate that there could be a significant risk of tick attacks on human population in Cuban ecosystems and tourists from Russia definitely share this risk. Indeed, there are numerous species of hard ticks inhabiting various biotopes, including urban and suburban areas and, probably, places of historical and recreational interest. However, in spite of the significant advance in current research, the information on tick and tick-borne infections in Cuba is still incomplete. Thus, the data on modern geographical distribution, population density and structure and ecological characteristics of Cuban Ixodid ticks are very limited. For example, the spatial distribution and abundance of endemic tick I. capro-mydis was described for the last time about 50 years ago [3]. There are no data available on attack rate of ticks on human hosts and the associated risk of tick-borne infections. The Lyme disease is still not confirmed for Cuba and no data about clinical cases of this disease are published [9], though there are serological findings that indicate the presence of this pathogen in Cuban ecosystems. The diversity and prevalence of tick-borne pathogens in Cuban ticks are also not fully described. Even for confirmed microorganisms like A. marginale, B. bovis and B. bigemina the additional studies are recommended [34]. All this information is critical to evaluate the threat of the tick for human health. Thus, extended ecological and epidemiological research will improve our knowledge
about tick-borne infections in Cuba and will provide the proper urgent diagnostics and prevention of tick-borne diseases in the bitten humans. Such research will also be a significant contribution to further improvement of the healthcare in the Republic of Cuba.
REFERENCES
1. Álvarez V, Gonzalez AC. (1991). The critical condition of hutias in Cuba. Oryx, 25, 206-208.
2. Barros-Battesti DM, Hernández MR, Famadas KM, Onofrio VC, Beati L, Guglielmone AA. (2009). The Ixodid ticks (Acari: Ixodidae) of Cuba. Systematic & Applied Aca-rology, 14, 101-128.
3. Cerny V. (1966). Nueva espécie de garrapata Del género Ixodes Latreille (Ixodoidea, Ixodidae) em la jutía conga de la Isla de Pinos. Poeyana, 24, 1-9.
4. Corona B, Machado H, Rodríguez M, Martínez S. (2009). Characterization of recombinant MSP5 Anaplasma marginale Havana isolate. Braz J Microbiol, 40 (4), 972-979.
5. Danchinova GA, Khasnatinov MA, Zlobin VI, Ko-zlova IV, Verkhozina MM, Sountsova OV, Shulunov SS, Abmed D, Bataa J, Bat-Ochir D, Tsend N, Badueva LN, Lisak OV, Gorina MO. (2006). Ixodid ticks in Southern part of Eastern Siberia and Mongolia and their spontaneous infectiveness by infectious agents. Bulletin of Siberian Medicine, 5 (S1), 137-143.
6. Danchinova GA, Liapunov AV, Khasnatinov MA, Tchaporgina ЕА, Arbatskaya EV, Petrova IV, Savelkaeva MV, Gorbunova EL, Tunik TV. (2012). Eco-geographic characteristics of appealability of people, suffered from tick bite in Irkutsk region and in other territories. Siberian Medical Journal (Irkutsk), 111 (4), 64-67.
7. Dantas-Torres F. (2010). Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors, 3, 26. doi: 10.1186/1756-3305-3-26.
8. Dantas-Torres F, Latrofa MS, Annoscia G, Gian-nelli A, Parisi A, Otranto D. (2013). Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasit Vectors, 6, 213. doi: 10.1186/1756-3305-6-213.
9. Dessau RB. (2012). Infection due to Borrelia burgdorferi most likely does not occur in Cuba. Braz J Infect Dis, 16 (4), 404.
10. Estrada-Peña A, Guglielmone AA, Mangold AJ. (2004). The distribution and ecological preferences of the tick Amblyomma cajennense (Acari: Ixodidae), an ectoparasite of humans and other mammals in the Americas. Ann Trop Med Parasitol, 98 (3), 283-292.
11. Filippova NA. (1977). Ixodid ticks of the subfamily Ixodinae. Fauna of Russia and adjacent countries. Arachni-da, 4 (4), 396. (In Russian)
12. Filippova NA. (1997). Ixodid ticks of the subfamily Amblyomminae. The fauna of Russia, 4, 436. (In Russian)
13. Gon^alves DD, Carreira T, Nunes M, Benitez A, Lopes-Mori FM, Vidotto O, de Freitas JC, Vieira ML. (2014). First record of Borrelia burgdorferi B31 strain in Dermacentor nitens ticks in the northern region of Parana (Brazil). Braz J Microbiol, 44 (3), 883-887.
14. Gray JS, Dautel H, Estrada-Pena A, Kahl O, Lin-dgren E. (2009). Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip Perspect Infect Dis, 12. doi: 10.1155/2009/593232.
15. Guglielmone AA, Beati L, Barros-Battesti DM, Labruna MB, Nava S, Venzal JM, Mangold AJ, Szabó MPJ, Martins JR., González-Acuña D, Estrada-Peña A. (2006). Ticks (Ixodoidea) on humans in South America. Exp Appl Acarol, 40, 83-100.
16. Guglielmone AA, Nava S. (2010). Hosts of Amblyomma dissimile Koch, 1844 and Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae). Zootaxa, 2541, 27-49.
17. Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. (2014). The hard ticks of the world. Springer Netherlands, 738 p. doi: 10.1007/978-94-007-7497-1.
18. Hubalek Z. (2009). Epidemiology of Lyme bor-reliosis. Curr Probl Dermatol, 37, 31-50.
19. Hubálek Z, Rudolf I. (2012). Tick-borne viruses in Europe. Parasitol Res, 111 (1), 9-36.
20. Dantas-Torres F, Otranto D. (2015). Further thoughts on the taxonomy and vector role of Rhipicephalus sanguineus group ticks. Vet Parasitol, 208 (1-2), 9-13.
21. Ismail N, Bloch KC, McBride JW. (2010). Human ehrlichiosis and anaplasmosis. Clin Lab Med, 30 (1), 261-292.
22. Khasnatinov MA, Liapunov AV, Manzarova EL, Kulakova NV, Petrova IV, Danchinova GA. (2016). The diversity and prevalence of hard ticks attacking human hosts in Eastern Siberia (Russian Federation) with first description of invasion of non-endemic tick species. Parasitol Res, 115 (2), 501-510.
23. Kolonin GV. (1981). The hard ticks of the world. Genera: Ixodes. Moscow, 114 p.
24. Korenberg EI, Lebedeva NN. (1969). Distribution and some general features of the ecology of Ixodes trian-guliceps Bir. in the Soviet Union. Folia Parasitological, 16, 143-152.
25. Korenberg E, Likhacheva T. (2006). Analysis of the long-term dynamics of tick-borne encephalitis (TBE) and Ixodid tick-borne borrelioses (ITBB) morbidity in Russia. Int J Med Microbiol, 296 (S1), 54-58.
26. Lyapunov AV, Khasnatinov MA, Arbatskaya EV, Danchinova GA. (2012). Findings of Amblyomma america-num L., 1758 in the Territory of Eastern Siberia (Russia). Problems of Particularly Dangerous Infections, 1 (111), 99-101. (In Russian)
27. Nowak-Chmura M. (2014). A biological/medical review of alien tick species (Acari: Ixodida) accidentally transferred to Poland. Ann Parasitol, 60 (1), 49-59.
28. Phillips R, Ayensu E, Beaver B, Benirschke K, Crawford R. (1991). Micro livestock: little known small animals with a promising economic future. Available at: https://www.nap.edu/read/1831/chapter/27?ter-m=hutia (date of access 21.03.2018).
29. Rodrigues VDS, Garcia MV, Cruz BC, Maciel WG, Zimmermann NP, Koller WW, Barros JC, Andreotti R. (2017). Life cycle and parasitic competence of Dermacentor nitens Neumann, 1897 (Acari: Ixodidae) on different animal species. Ticks Tick Borne Dis, 8 (3), 379-384. doi: 10.1016/j.ttbdis.2016.12.014.
30. Rodriguez I, Fernandez C, Sanchez L, Martinez B, Siegrist HH, Lienhard R. (2012). Prevalence of antibodies to Borrelia burgdorferi sensu stricto in humans from a Cuban village. Braz J Infect Dis, 16, 82-85.
31. Rodríguez I, Burri C, Noda AA, Douet V, Gern L. (2015). Multiplex PCR for molecular screening of Borrelia
burgdorferi sensu lato, Anaplasma spp. and Babesia spp. Ann Agric Environ Med, 22 (4), 642-646.
32. Russia Tourism: official website. Statistical indicators of mutual trips of citizens of the russian federation and citizens of foreign states. Available at: https://www. russiatourism.ru/contents/statistika/statisticheskie-po-kazateli-vzaimnykh-poezdok-grazhdan-rossiyskoy-fed-eratsii-i-grazhdan-inostrannykh-gosudarstv/ (date of access 21.03.2018).
33. Scoles GA, Ueti MW. (2013). Amblyomma cajen-nense is an intrastadial biological vector of Theileria equi. Parasit Vectors, 6 (1), 306. doi: 10.1186/1756-3305-6-306.
34. Scott JD, Durden LA. (2015). Amblyomma dis-simile Koch (Acari: Ixodidae) parasitizes bird captured in Canada. Syst Appl Acarology, 20 (8), 854-860
35. Suárez Hernández M, Alonso Castellano M, Peláez Martínez R, Sánchez Pérez B, Bravo González JR, Sánchez Sibello A. (1997). Investigation of Babesia in farm workers and blood donors in the province of Ciego de Avila. Rev Cubana Med Trop, 49 (2), 130-135.
36. Vatansever Z, Gargili A, Aysul NS, Sengoz G, Estrada-Peña A. (2008). Ticks biting humans in the urban area of Istanbul. Parasitol Res, 102 (3), 551-553.
37. Vigueras Pérez J. (1934). On the ticks of Cuba, with description of a new species, Amblyomma Torrei, from Cyclura Macleayi Gray Psyche.JEntomol, 41 (1), 1318. http://dx.doi.org/10.1155/1934/32624.
38. Woods CA, Kilpatrick CW. (2005). Infraorder Hystricognathi. Mammal Species of the World: A Taxonomic and Geographic Reference, 2, 3, 1538-1600.
Information about the authors
Khasnatinov Maxim Anatolyevich - Candidate of Biological Sciences, Leading Research Officer at the Laboratory of Transmissive Infections, Scientific Centre for Family Health and Human Reproduction Problems (664003, Irkutsk, ul. Timiryazeva, 16; tel. (3952) 33-39-71; e-mail: [email protected]) © http://orcid.org/0000-0002-8441-3640
Rychkova Lyubov Vladimirovna - Doctor of Medical Sciences, Director, Scientific Centre for Family Health and Human Reproduction Problems (tel. (3952) 20-73-67; e-mail: [email protected])
Rodriguez Gonzales Islay - PhD, Institute of Tropical Medicine Pedro Kouri (P.O.B. 601, Marianao 13, Habana, Cuba; e-mail: [email protected])
Corona GonzalesBelkis - PhD, National Centre for Animal and Plant Health (Apartado 10, 32700, San José de las Lajas, La Habana, Cuba; e-mail: [email protected])
Danchinova Galina Anatolyevna - Doctor of Biological Sciences, Head of the Laboratory of Transmissive Infections, Scientific Centre for Family Health and Human Reproduction Problems (e-mail: [email protected])
