Tularemia in the world

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Abstract

Here we review the data on the global spread of tularemia — a natural focal, especially dangerous human and animal infection caused by the bacterium Francisella tularensis. Strains of the most virulent F. tularensis subspecies tularensis circulate solely in the North America, whereas less virulent F. tularensis subspecies holarctica is found in Europe, Asia (Japan), North America, Australia (especially Tasmania). Isolates of this subspecies are isolated in territories of various climatic zones — from subarctic to subtropical, featured with diverse biocenoses in natural foci — from water to desert, with their unique hosts and carriers. Compared with the remaining subspecies of the tularemia causative agent, subspecies holarctica has a wide spread due to its ability to live in aquatic environment that markedly expands its distribution areas and shows higher ecological plasticity and stability. Infection of people by such causative agents occurs due to infected blood-sucking arthropods biting (mosquitoes, horseflies, ticks), intake of rodent-contaminated food and water, inhalation of air-dust aerosol bearing tularemia pathogen transmitted from sick rodents, as well as after direct contact with infected animals (hunting, pet care, carcass cutting). Different routes of the pathogen transmission in various countries are discussed. The peak prevalence of tularemia is observed in the North America (USA) and Europe (Sweden and Finland), as well as in Asia (Turkey). Since the mid-20th century, incidence rate of tularemia has been profoundly decreased in the Russian Federation and Kazakhstan due to preventing populations in tularemia-enzootic territories as well as those at risk of contact. In the last years, 31 European countries as well as Turkey and Japan have begun to conduct mandatory registration of tularemia cases due to an opportunity of using the pathogen for bioterrorism. The geographical distribution of the main tularemia microbe phylogenetic populations and subpopulations is demonstrated. The peak diversity of F. tularensis subsp. holarctica strains in a single country was registered in China. The major ecology- and epidemiology-related features of the tularemia causative agent are noted.

About the authors

T. Yu. Kudryavtseva

State Research Center for Applied Microbiology and Biotechnology

Email: tomakud@yandex.ru

PhD (Biology), Senior Researcher, Department of Especially Dangerous Infections, State Research Center for Applied Microbiology and Biotechnology.

142279, Moscow Region, Serpukhov District, Obolensk.

Россия

A. N. Mokrievich

State Research Center for Applied Microbiology and Biotechnology

Author for correspondence.
Email: mokrievich@obolensk.org
ORCID iD: 0000-0003-3675-8780

Alexander N. Mokrievich - PhD, MD (Medicine), Head of the Department of Especially Dangerous Infections, State Research Center for Applied Microbiology and Biotechnology.

142279, Moscow Region, Serpukhov District, Obolensk.

Phone: +7 (496) 736-01-17 (office); +7 (905) 780-61-61 (mobile)

Россия

References

  1. В Латвии несколько детей заболели опасной болезнью — туляремией // Наш город: новости Даугавпилса. 2012. URL: https://gorod.lv/novosti/166079-v-latvii-neskolko-detei-zaboleli-opasnoi-infektsiei-tulyaremiei (11.11.2020).
  2. Данчинова Г.А., Хаснатинов М.А., Злобин В.И., Козлова И.В., Верхозина М.М., Сунцова О.В., Шулунов С.С., Абмэд Д., Батаа Ж., Бат-Очир Д., Цэнд Н., Бадуева Л.Б., Лисак О.В., Горина М.О. Иксодовые клещи юга Восточной Сибири и Монголии и их спонтанная зараженность возбудителями природно-очаговых трансмиссивных инфекций // Бюллетень сибирской медицины. 2006. Т. 5, № S1. С. 137—143. doi: 10.20538/1682-03632006-137-143
  3. Куница Т.Н., Избанова У.А., Ерубаев Т.К., Аязбаев Т.З., Мека-Меченко В.Г., Абдел З.Ж., Мека-Меченко Т.В., Садовская В.П. Природная очаговость туляремии в Казахстане. Алматы: КНЦКЗИ, 2019. 97 с.
  4. Куница Т.Н., Избанова У.А., Мека-Меченко В.Г., Майканов Н.С., Садовская В.П. Эпизоотическая активность природных очагов туляремии Казахстана на приграничной с Россией территории // Дальневосточный журнал инфекционной патологии. 2014. № 25. С. 63—65.
  5. Мещерякова И.С., Коренберг Э.И., Tserennorov D., Михайлова Т.В., Кормилицына М.И., Batjav D., Dagvadorj Y., Демидова Т.Н., Otgonbaatar D., Enkhbold N., Mendamar L. Выявление природных очагов туляремии на территории Монголии // Журнал микробиологии, эпидемиологии и иммунобиологии. 2011. № 5. С. 31—36. , Epidemiology and Immunobiology, 2011, no. 5, pp. 31—36. (In Russ.)]
  6. Мокриевич А.Н., Тимофеев В.С., Кудрявцева Т.Ю., Уланова Г.И., Карбышева С.Б., Миронова Р.И., Вахрамеева Г.М., Губарева Т.И., Павлов В.М., Дятлов И.А. Выделение среднеазиатского подвида туляремийного микроба на территории Алтайского края // Проблемы особо опасных инфекций. 2013. № 1. С. 66—69.
  7. Небогаткин И., Новохатний Ю., Выдайко Н., Билоник О., Свита В. Туляремия в Украине, современное ландшафтно-географичесское деление очагов, трансграничный аспект // Ветеринарная медицина. 2017. № 103. С. 56—57.
  8. Попов В.П., Мезенцев В.М., Бирковская Ю.А., Безсмертный В.Е., Таджидинов В.О., Тараканов Т.А., Фольмер А.Я., Юрченко Ю.А., Мищенко А.И., Лопатин А.А. Трансграничные природные очаги туляремии Российской Федерации и Республики Казахстан // Карантинные и зоонозные инфекции в Казахстане. 2019. Т. 38, № 1. С. 95—105.
  9. Почебут М.И. О профилактике туляремии. Городская поликлиника № 1 г. Гродно. URL: http://gp1.by/pages/o-profilaktike-tulyaremii.html (11.11.2020)
  10. Прилуцкий А.С., Роговая Ю.Д., Зубко В.Г. Туляремия, этиология, эпидемиология, вакцинопрофилактика // Университетская клиника. 2017. Т. 13, № 2. С. 231—240.
  11. Цвирко Л.С., Селькина Е.С., Сенковец Т.А., Козлов А.М. Туляремия в белорусском Полесье. Часть II. Период 2001— 2015 гг. // Вестник Полесского гос. ун-та. Сер. природоведч. наук. 2016. № 2. С. 34—40.
  12. Afset J.E., Larssen K.W., Bergh K., Larkeryd A., Sjodin A., Johansson A., Forsman M. Phylogeographical pattern of Francisella tularensis in a nationwide outbreak of tularaemia in Norway, 2011. Euro Surveill., 2015, 20 (19): 21125. doi: 10.2807/1560-7917.ES2015.20.19.21125
  13. Akhvlediani N., Burjanadze I., Baliashvili D., Tushishvili T., Broladze M., Navdarashvili A., Dolbadze S., Chitadze N., Topuridze M., Imnadze P., Kazakhashvili N., Tsertsvadze T., Kuchuloria T., Akhvlediani T., McNutt L.A., Chanturia G. Tularemia transmission to humans: a multifaceted surveillance approach. Epidemiol. Infect., 2018, vol. 146, no. 16, pp. 2139-2145. doi: 10.1017/S0950268818002492
  14. Ariza-Miguel J., Johansson A., Fernandez-Natal M.I., Martinez-Nistal C., Orduna A., Rodriguez-Ferri E.F., Hernandez M., Rodriguez-Lazaro D. Molecular Investigation of tularemia outbreaks, Spain, 1997—2008. Emerg. Infect. Dis., 2014, vol. 20, no. 5, pp. 754-761. doi: 10.3201/eid2005.130654
  15. Bielawska-Drozd A., Cieslik P., Zakowska D., Glowacka P., Wlizlo-Skowronek B., Zi^ba P., Zdun A. Detection of Coxiella burnetii and Francisella tularensis in tissues of wild-living animals and in ticks of North-West Poland. Pol. J. Microbiol., 2018, vol. 67, no. 4, pp. 529-534. doi: 10.21307/pjm-2018-059
  16. Bundesamt fur Gesundheit BAG. BAG-Bulletin 2016, 2017, 2018. Das Portal der Schweizer Regierung. URL: https://www.bag.admin.ch/bag/de/home/das-bag/publikationen/periodika/bag-bulletin.html (11.11.2020)
  17. Chanturia G., Birdsell D.N., Kekelidze M., Zhgenti E., Babuadze G., Tsertsvadze N., Tsanava S., Imnadze P., Beckstrom-Sternberg S.M., Beckstrom-Sternberg J.S., Champion M.D., Sinari S., Gyuranecz M., Farlow J., Pettus A.H., Kaufman E.L., Busch J.D., Pearson T., Foster J.T., Vogler A.J., Wagner D.M., Keim P. Phylogeography of Francisella tularensis subspecies hol-arctica from the country of Georgia. BMC Microbiol., 2011, vol. 11, no. 1: 139. doi: 10.1186/1471-2180-11-139
  18. Clark D.V., Ismailov A., Seyidova E., Hajiyeva A., Bakhishova S., Hajiyev H., Nuriyev T., Piraliyev S., Bagirov S., Aslanova A., Debes A.K., Qasimov M., Hepburn M.J. Seroprevalence of tularemia in rural Azerbaijan. Vector Borne Zoonotic Dis., 2012, vol. 12, no. 7, pp. 558-563. doi: 10.1089/vbz.2010.0081
  19. Decors A., Lesage C., Jourdain E., Giraud P., Houbron P., Vanhem P., Madani N. Outbreak of tularaemia in brown hares (Lepus europaeus) in France, January to March 2011. Euro Surveill., 2011, vol. 16, no. 28: 19913.
  20. Desvars A., Furberg M., Hjertqvist M., Vidman L., Sjostedt A., Ryden P., Johansson A. Epidemiology and ecology of tularemia in Sweden, 1984—2012. Emerg. Infect. Dis, 2015, vol. 21, no. 1, pp. 32-39. doi: 10.3201/eid2101.140916
  21. Desvars-Larrive A., Liu X., Hjertqvist M., Sjostedt A., Johansson A., Ryden P. High-risk regions and outbreak modelling of tularemia in humans. Epidemiol. Infect., 2017, vol. 145, no. 3, pp. 482-490. doi: 10.1017/S0950268816002478
  22. Dryselius R., Hjertqvist M., Makitalo S., Lindblom A., Lilja T., Eklof D., Lindstrom A. Large outbreak of tularaemia, central Sweden, July to September 2019. Euro Surveill., 2019, vol. 24, no. 42: 1900603. doi: 10.2807/1560-7917.ES.2019.24.42.1900603
  23. Duzlu O., Yildirim A., Inci A., Gumussoy K.S., Ciloglu A., Onder Z. Molecular investigation of Francisella-like endosymbiont in ticks and Francisella tularensis in Ixodid ticks and mosquitoes in Turkey. Vector Borne Zoonotic Dis., 2016, vol. 16, no. 1, pp. 26-32. doi: 10.1089/vbz.2015.1818
  24. Eden J.S., Rose K., Ng J., Shi M., Wang Q., Sintchenko V., Holmes E.C. Francisella tularensis ssp. holarctica in Ringtail Possums, Australia. Emerg. Infect. Dis., 2017, vol. 23, no. 7, pp. 1198-1201. doi: 10.3201/eid2307.161863
  25. Elashvili E., Kracalik I., Burjanadze I., Datukishvili S., Chanturia G., Tsertsvadze N., Beridze L., Shavishvili M., Dzneladze А., Grdzelidze M., Imnadze P., Pearson A., Blackburn J.K. Environmental monitoring and surveillance of rodents and vectors for Francisella tularensis following outbreaks of human tularemia in Georgia. Vector Borne Zoonotic Dis., 2015, vol. 15, no. 10, pp. 633-636. doi: 10.1089/vbz.2015.1781
  26. Eliasson H., Back E. Tularaemia in an emergent area in Sweden: an analysis of 234 cases in five years. Scand. J. Infect. Dis., 2007, vol. 39, no. 10, pp. 880-889. doi: 10.1080/00365540701402970
  27. Erdem H., Ozturk-Engin D., Yesilyurt M., Karabay O., Elaldi N., Celebi G., Korkmaz N., Guven T., Sumer S., Tulek N., Ural O., Yilmaz G., Erdinc S., Nayman-Alpat S., Sehmen E., Kader C., Sari N., Engin A., Cicek-Senturk G., Ertem-Tuncer G., Gulen G., Duygu F., Ogutlu A., Ayaslioglu E., Karadenizli A., Meric M., Ulug M., Ataman-Hatipoglu C., Sirmatel F., Cesur S., Comoglu S., Kadanali A., Karakas A., Asan A., Gonen I., Kurtoglu-Gul Y., Altin N., Ozkanli S., Yilmaz-Karadag F., Cabalak M., Gencer S., Umut Pekok A., Yildirim D., Seyman D., Teker B., Yilmaz H., Yasar K., Inanc Balkan I., Turan H., Uguz M., Kilic S., Akkoyunlu Y., Kaya S., Erdem A., Inan A., Cag Y., Bolukcu S., Ulu-Kilic A., Ozgunes N., Gorenek L., Batirel A., Agalar C. Evaluation of tularaemia courses: a multicentre study from Turkey. Clin. Microbiol. Infect., 2014, vol. 20, no. 12, pp. O1042-O1051. doi: 10.1111/1469-0691.12741
  28. Faber M., Heuner K., Jacob D., Grunow R. Tularemia in Germany — a re-emerging zoonosis. Front. Cell. Infect. Microbiol., 2018, vol. 8, no. 40. doi: 10.3389/fcimb.2018.00040
  29. Farlow J., Wagner D.M., Dukerich M., Stanley M., Chu M., Kubota K., Petersen J., Keim P. Francisella tularensis in the United States. Emerg. Infect. Dis., 2005, vol. 11, no. 12, pp. 1835-1841. doi: 10.3201/eid1112.050728
  30. Forminska K., Zasada A.A., Rastawicki W., Smietanska K., Bander D., Wawrzynowicz-Syczewska M., Yanushevych M., Niscigorska-Olsen J., Wawszczak M. Increasing role of arthropod bites in tularaemia transmission in Poland — case reports and diagnostic methods. Ann. Agric. Environ. Med., 2015, vol. 22, no. 3, pp. 443-446. doi: 10.5604/12321966.11677
  31. Forsman M., Henningson E.W., Larsson E., Johansson T., Sandstrom G. Francisella tularensis does not manifest virulence in viable but non-culturable state. FEMS Microbiol. Ecol., 2000, vol. 31, no. 3, pp. 217-224. doi: 10.1111/j.1574-6941.2000.tb00686.x
  32. Fujita O., Uda A., Hotta A., Okutani A., Inoue S., Tanabayashi K., Yamada A. Genetic diversity of Francisella tularensis subspecies holarctica strains isolated in Japan. Microbiol. Immunol., 2008, vol. 52, no. 5, pp. 270-276. doi: 10.1111/j.1348-0421.2008.00036.x
  33. Genchi M., Prati P., Vicari N., Manfredini A., Sacchi L., Clementi E., Bandi C., Epis S., Fabbi M. Francisella tularensis: no evidence for transovarial transmission in the tularemia tick vectors Dermacentor reticulatus and Ixodes ricinus. PLoS One, 2015, vol. 10, no. 8: e0133593. doi: 10.1371/journal.pone.0133593
  34. Gerhart J.G., Auguste Dutcher H., Brenner A.E., Moses A.S., Grubhoffer L., Raghavan R. Multiple acquisitions of pathogen-derived Francisella endosymbionts in soft ticks. Genome Biol. Evol., 2018, vol. 10, no. 2, pp. 607-615. doi: 10.1093/gbe/evy021
  35. Grunow R., Kalaveshi A., Kuhn A., Mulliqi-Osmani G., Ramadani N. Surveillance of tularaemia in Kosovo, 2001 to 2010. Euro Surveill., 2012, vol. 17, no. 28: 20217. doi: 10.2807/ese.17.28.20217-en
  36. Gurcan S. Epidemiology of tularemia. Balkan. Med. J., 2014, vol. 31, no. 1, pp. 3-10. doi: 10.5152/balkanmedj.2014.13117
  37. Gurycova D., Tinakova K., Vyrostekova V., Gacikova E. The incidence of tularemia in Slovakia in 1997—2008. Epidemiol. Mikrobiol. Imunol., 2010, vol. 59, no. 1, pp. 39-44.
  38. Gyuranecz M., Szeredi L., Makrai L., Fodor L., Meszaros A.R., Szepe B., Fuleki M., Erdelyi K. Tularemia of European brown hare (Lepus europaeus): a pathological, histopathological, and immunohistochemical study. Vet. Pathol., 2010, vol. 47, no. 5, pp. 958-963. doi: 10.1177/0300985810369902
  39. Gyuranecz M., Reiczigel J., Krisztalovics K., Monse L., Szabone G.K., Szilagyi A., Szepe B., Makrai L., Magyar T., Bhide M., Erdelyi K. Factors influencing emergence of tularemia, Hungary, 1984—2010. Emerg. Infect. Dis., 2012, vol. 18, no. 8, pp. 13791381. doi: 10.3201/eid1808.111826
  40. Hennebique A., Boisset S., Maurin M. Tularemia as a waterborne disease: a review. Emerg. Microbes Infect., 2019, vol. 8, pp. 10271042. doi: 10.1080/22221751.2019.1638734
  41. Hestvik G., Warns-Petit E., Smith L.A., Fox N.J., Uhlhorn H., Artois M., Hannant D., Hutchings M.R., Mattsson R., Yon L., Gavier-Widen D. The status of tularemia in Europe in a one-health context: a review. Epidemiol. Infect., 2015, vol. 143, no. 10, pp. 2137-2160. doi: 10.1017/S0950268814002398
  42. Hightower J., Kracalik I.T., Vydayko N., Goodin D., Glass G., Blackburn J.K. Historical distribution and host-vector diversity of Francisella tularensis, the causative agent of tularemia, in Ukraine. Parasit. Vectors, 2014, vol. 7, no. 453. doi: 10.1186/s13071-014-0453-2
  43. Huber B., Escudero R., Busse H.J., Seibold E., Scholz H.C., Anda P., Kampfer P., Splettstoesser W.D. Description of Francisella hispaniensis sp. nov., isolated from human blood, reclassification of Francisella novicida (Larson et al. 1955) Olsufiev et al. 1959. as Francisella tularensis subsp. novicida comb. nov. and emended description of the genus Francisella. Int. J. Syst. Evol. Microbiol., 2010, vol. 60, no. 8, pp. 1887-1896. doi: 10.1099/ijs.0.015941-0
  44. Janse I., van der Plaats R.Q.J., de Roda Husman A.M., van Passel M.W.J. Environmental surveillance of zoonotic Francisella tularensis in the Netherlands. Front. Cell. Infect. Microbiol., 2018, vol. 8, no. 140. doi: 10.3389/fcimb.2018.00140
  45. Johansson A., Larkeryd A., Widerstrom M., Mortberg S., Myrtannas K., Ohrman C., Birdsell D., Keim P., Wagner D.M., Forsman M., Larsson P. An outbreak of respiratory tularemia caused by diverse clones of Francisella tularensis. Clin. Infect. Dis., 2014, vol. 59, no. 11, pp. 1546-1553. doi: 10.1093/cid/ciu621
  46. Jones B.D., Faron M., Rasmussen J.A., Fletcher J.R. Uncovering the components of the Francisella tularensis virulence stealth strategy. Front. Cell. Infect. Microbiol., 2014, vol. 4, no. 32. doi: 10.3389/fcimb.2014.00032
  47. Kang C., Wang Z., Han W. An epidemiological investigation on the first epidemic ofhuman tularemia in China. Chin. J. Epidemiol., 1980, vol. 1, pp. 248-251.
  48. Kantardjiev T., Ivanov I., Velinov T., Padeshki P., Popov B., Nenova R., Mincheff M. Tularemia outbreak, Bulgaria, 1997-2005. Emerg. Infect. Dis., 2006, vol. 12, no. 4, pp. 678-680. doi: 10.3201/eid1204.050709
  49. Karadenizli A., Forsman M., §im§ek H., Taner M., Ohrman C., Myrtennas K., Larkeryd A., Johansson A., Ozdemir L., Sjodin A. Genomic analyses of Francisella tularensis strains confirm disease transmission from drinking water sources, Turkey, 2008, 2009 and 2012. Euro Surveill., 2015, vol. 20, no. 21: 21136. doi: 10.2807/1560-7917.es2015.20.21.21136
  50. Karlsson E., Golovliov I., Larkeryd A., Granberg M., Larsson E., Ohrman C., Niemcewicz M., Birdsell D., Wagner D.M., Forsman M., Johansson A. Clonality of erythromycin resistance in Francisella tularensis. J. Antimicrob. Chemother., 2016, vol. 71, pp. 2815-2823. doi: 10.1093/jac/dkw235
  51. Kaysser P., Seibold E., Matz-Rensing K., Pfeffer M., Essbauer S., Splettstoesser W.D. Re-emergence of tularemia in Germany: presence of Francisella tularensis in different rodent species in endemic areas. BMC Infect. Dis., 2008, vol. 8: 157. doi: 10.1186/14712334-8-157
  52. Kili? S., Birdsell D.N., Karagoz A., £elebi B., Bakkaloglu Z., Arikan M., Sahl J.W., Mitchell C., Rivera A., Maltinsky S., Keim P., Ustek D., Durmaz R., Wagner D.M. Water as source of Francisella tularensis infection in humans. Turkey. Emerg. Infect. Dis., 2015, vol. 21, no. 12, pp. 2213-2216. doi: 10.3201/eid2112.150634
  53. Kill? S., £elebi B., Acar B., Ata§ M. In vitro susceptibility of isolates of Francisella tularensis from Turkey. Scand. J. Infect. Dis., 2013, vol. 45, pp. 337-341. doi: 10.3109/00365548.2012.751125
  54. Koene M., Rijks J., Maas M., Ruuls R., Engelsma M., van Tulden P., Kik M., IJzer J., Notermans D., de Vries M., Fanoy E., Pijnacker R., Spierenburg M., Bavelaar H., Berkhout H., Sankatsing S., Diepersloot R., Myrtennas K., Granberg M., Forsman M., Roest H-J., Grone A. Phylogeographic distribution of human and hare Francisella tularensis subsp. holarctica strains in the Netherlandsand and its pathology in European brown hares (Lepus europaeus). Front. Cell. Infect. Microbiol., 2019, vol. 9: 11. doi: 10.3389/fcimb.2019.00011
  55. Kugeler K.J., Mead P.S., Janusz A.M., Staples J.E., Kubota K.A., Chalcraft L.G., Petersen J.M. Molecular epidemiology of Francisella tularensis in the United States. Clin. Infect. Dis., 2009, vol. 48, no. 7, pp. 863-870. doi: 10.1086/597261
  56. Lu Y., Yu Y., Feng L., Li Y., He J., Zhu H., Duan Q., Song L. Phylogeography of Francisella tularensis from Tibet, China: evidence for an asian origin and radiation of holarctica-type tularemia. Ticks Tick Borne Dis., 2016, vol. 7, no. 5, pp. 865-868. doi: 10.1016/j.ttbdis.2016.04.001
  57. Lundstrom J.O., Andersson A.C., Backman S., Schafer M.L., Forsman M., Thelaus J. Transstadial transmission of Francisella tularensis holarctica in mosquitoes, Sweden. Emerg. Infect. Dis., 2011, vol. 17, no. 5, pp. 794-799. doi: 10.3201/eid1705.100426
  58. Macela A., Stulik J., Krocova Z., Kroca M., Kubelkova K. Francisella tularensis — 100 years: tularemia research in former Czechoslovakia and Czech Republic. Mil. Med. Sci. Lett. (Voj. Zdrav. Listy), 2012, vol. 81, no. 2, pp. 46-55. doi: 10.31482/mmsl.2012.006
  59. Mailles A., Vaillant V. 10 years of surveillance of human tularaemia in France. Euro Surveill., 2014, vol. 19, no. 45: 20956. doi: 10.2807/1560-7917.es2014.19.45.20956
  60. Mani R.J., Metcalf J.A., Clinkenbeard K.D. Amblyomma americanum as a bridging vector for human infection with Francisella tularensis. PLoS One, 2015, vol. 10, no. 6: e0130513. doi: 10.1371/journal.pone.0130513
  61. Mani R.J., Morton R.J., Clinkenbeard K.D. Ecology of tularemia in Central US Endemic Region. Curr. Trop. Med. Rep., 2016, vol. 3, no. 3, pp. 75-79. doi: 10.1007/s40475-016-0075-1
  62. Maurin M., Pelloux I., Brion J.P., Del Bano J.N., Picard A. Human tularemia in France, 2006—2010. Clin. Infect. Dis., 2011, vol. 53, vol. 10: e133-41. doi: 10.1093/cid/cir612
  63. Maurin M., Gyuranecz M. Tularaemia: clinical aspects in Europe. Lancet Infect. Dis., 2016, vol. 16, no. 1, pp. 113-124. doi: 10.1016/S1473-3099(15)00355-2
  64. Melikjanyan S., Palayan K., Vanyan A., Avetisyan L., Bakunts N., Kotanyan M., Guerra M. Human cases of tularemia in Armenia, 1996-2012. Am. J. Trop. Med. Hyg, 2017, vol. 97, no. 3,pp. 819-825. doi: 10.4269/ajtmh.16-0605
  65. Origgi F.C., Frey J., Pilo P. Characterisation of a new group of Francisella tularensis subsp. holarctica in Switzerland with altered antimicrobial susceptibilities, 1996 to 2013. Euro Surveill., 2014, vol. 19, no. 29: 20858. doi: 10.2807/1560-7917.es2014.19.29.20858
  66. Ozsurekci Y., Birdsell D.N., £elik M., Karadag-Oncel E., Johansson A., Forsman M., Vogler A.J., Keim P., Ceyhan M., Wagner D.M. Diverse Francisella tularensis strains and oropharyngeal tularemia, Turkey. Emerg. Infect. Dis., 2015, vol. 21, no. 1, pp. 173-175. doi: 10.3201/eid2101.141087
  67. Pang Z., Geng Y., Xiao Y. Investigation of the first outbreak of tularemia in Shandong Peninsula. Chin. J. Epidemiol., 1987, vol. 5, pp. 261-263.
  68. Park C.H., Nakanishi A., Hatai H., Kojima D., Oyamada T., Sato H., Kudo N., Shindo J., Fujita O., Hotta A., Inoue S., Tanabayashi K. Pathological and microbiological studies of Japanese Hare (Lepus brachyurus angustidens) naturally infected with Francisella tularensis subsp. holarctica. J. Vet. Med. Sci., 2009, vol. 71, no. 12, pp. 1629-1635. doi: 10.1292/jvms.001629
  69. Pikula J., Beklova M., Holesovska Z., Treml F. Prediction of possible distribution of tularemia in the Czech Republic. Vet. Med. — Czech, 2004, vol. 49, no. 2, pp. 61-64.
  70. Pikula J., Treml F., Beklova M., Holesovska Z., Pikulova J. Ecological conditions of natural foci of tularaemia in the Czech Republic. Eur. J. Epidemiol., 2003, vol. 18, no. 11, pp. 1091-1095. doi: 10.1023/a:1026141619810
  71. Pilo P. Phylogenetic lineages of Francisella tularensis in animals. Front. Cell. Infect. Microbiol., 2018, vol. 8: 258. doi: 10.3389/fcimb.2018.00258
  72. Puente-Redondo V.A. de la, Blanco N.G. del, Gutierrez-Martin C.B., Garcia-Pena F.J., Rodriguez Ferri E.F. Comparison of different PCR approaches for typing of Francisella tularensis strains. J. Clin. Microbiol., 2000, vol. 38, no. 3, pp. 1016-1022.
  73. Qu P.H., Li Y., Salam N., Chen S.Y., Liu L., Gu Q., Fang B.Z., Xiao M., Li M., Chen C., Li W.J. Allofrancisella inopinata gen. nov. sp nov. and Allofrancisella frigidaquae sp nov., isolated from water-cooling systems, and transfer of Francisella guangzhouensis Qu et al 2013 to the new genus as Allofrancisella guangzhouensis comb. nov. Int. J. Syst. Evol. Microbiol., 2016, vol. 66, no. 11, pp. 4832-4838. doi: 10.1099/ijsem.0.001437
  74. Reintjes R., Dedushaj I., Gjini A., Jorgensen T.R., Cotter B., Lieftucht A., D'Ancona F., Dennis D.T., Kosoy M.A., Mulliqi-Osmani G., Grunow R., Kalaveshi A., Gashi L., Humolli I. Tularemia outbreak investigation in Kosovo: case control and environmental studies. Emerg. Infect. Dis., 2002, vol. 8, no. 1, pp. 69-73.
  75. Rodriguez-Pastor R., Escudero R., Vidal D., Mougeot F., Arroyo B., Lambin X., Vila-Coro A.M., Rodriguez-Moreno I., Anda P., Luque-Larena J.J. Density-dependent prevalence of Francisella tularensis in fluctuating vole populations, Northwestern Spain. Emerg. Infect. Dis., 2017, vol. 23, no. 8, pp. 1377-1379. doi: 10.3201/eid2308.161194
  76. Rossow H., Ollgren J., Hytonen J., Rissanen H., Huitu O., Henttonen H., Kuusi M., Vapalahti O. Incidence and seroprevalence of tularaemia in Finland, 1995 to 2013: regional epidemics with cyclic pattern. Euro Surveill., 2015, vol. 20, no. 33: 21209. doi: 10.2807/1560-7917.es2015.20.33.21209
  77. Rossow H., Ollgren J., Klemets P., Pietarinen I., Saikku J., Pekkanen E., Nikkari S., Syrjala H., Kuusi M., Nuorti J.P. Risk factors for pneumonic and ulceroglandular tularaemia in Finland: a population-based case-control study. Epidemiol. Infect., 2014, vol. 142, no. 10, pp. 2207-2216. doi: 10.1017/S0950268813002999
  78. Schulze C., Heuner K., Myrtennas K., Karlsson E., Jacob D., Kutzer P., GroBe K., Forsman M., Grunow R. High and novel genetic diversity of Francisella tularensis in Germany and indication of environmental persistence. Epidemiol. Infect., 2016, vol. 144, no. 14, pp. 3025-3036. doi: 10.1017/S0950268816001175
  79. Se elevan a 23 las personas afectadas por tularemia en provincia de Palencia. La Vanguardia. 2019. URL: https://www.lavan-guardia.com/vida/20190812/464008536428/se-elevan-a-23-las-personas-afectadas-por-tularemia-en-provincia-de-palencia.html (11.11.2020).
  80. Svensson K., Back E., Eliasson H., Berglund L., Granberg M., Karlsson L., Larsson P., Forsman M., Johansson A. Landscape epidemiology of tularemia outbreaks in Sweden. Emerg. Infect. Dis., 2009, vol. 15, no. 12, pp. 1937-1947. doi: 10.3201/eid1512.090487
  81. Tezer H., Ozkaya-Parlakay A., Aykan H., Erkocoglu M., Gulhan B., Demir A., Kanik-Yuksek S., Tapisiz A., Polat M., Kara S., Devrim I., Kilic S. Tularemia in children, Turkey, September 2009 — November 2012. Emerg. Infect. Dis., 2015, vol. 21, no. 1, pp. 1-7. doi: 10.3201/eid2101.131127
  82. Thelaus J., Andersson A., Broman T., Backman S., Granberg M., Karlsson L., Kuoppa K., Larsson E., Lundmark E., Lundstrom J.O., Mathisen P., Naslund J., Schafer M., Wahab T., Forsman M. Francisella tularensis subspecies holarctica occurs in swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding. Microb. Ecol., 2014, vol. 67, no. 1, pp. 96-107. doi: 10.1007/s00248-013-0285-1
  83. Timofeev V., Bakhteeva I., Titareva G., Kopylov P., Christiany D., Mokrievich A., Dyatlov I., Vergnaud G. Russian isolates enlarge the known geographic diversity of Francisella subsp. mediasiatica. PLoS One, 2017, vol. 12, no. 9:e0183714. doi: 10.1371/journal.pone.0183714
  84. Tularaemia. In: European Centre for Disease Prevention and Control. Annual Epidemiological Report for 2014. Stockholm: ECDC, 2016. URL: https://www.ecdc.europa.eu/sites/portal/files/documents/Tularaemia%20AER_0.pdf (11.11.2020).
  85. Tularaemia. In: European Centre for Disease Prevention and Control. Annual Epidemiological Report for 2017. Stockholm: ECDC, 2019. URL: https://ecdc.europa.eu/sites/portal/files/documents/tularaemia-annual-epidemiological-report-2017.pdf (11.11.2020).
  86. Vogler A.J., Birdsell D., Price L.B., Bowers J.R., Beckstrom- Sternberg S.M., Auerbach R.K., Beckstrom- Sternberg J.S., Johansson A., Clare A., Buchhagen J.L., Petersen J.M., Pearson T., Vaissaire J., Dempsey M.P., Foxall P., Engelthaler D.M., Wagner D.M., Keim P. Phylogeography of Francisella tularensis: global expansion of a highly fit clone. J. Bacteriol., 2009, vol. 191, no. 8, pp. 2474-2484. doi: 10.1128/JB.01786-08
  87. Wang Y., Peng Y., Hai R., Xia L., Li H., Zhang Z., Cai H., Liang Y., Shen X., Yu D., Birdsell D., Wagner D.M., Keim P. Diversity of Francisella tularensis subsp. holarctica lineages, China. Emerg. Infect. Dis., 2014, vol. 20, no. 7, pp. 1191-1194. doi: 10.3201/eid2007.130931
  88. Wang Y.H., Qiao F.Yu., Cao J., Peng Y., Li H., Xia L.X., Hai R. A case of Francisella tularensis subspecies holarctica in China. Ticks Tick Borne Dis., 2015, vol. 6, no. 6, pp. 802-804. doi: 10.1016/j.ttbdis.2015.07.007
  89. Williamson D.R., Dewan K.K., Patel T., Wastella C.M., Ning G., Kirimanjeswara G.S. A single mechanosensitive channel protects Francisella tularensis subsp. holarctica from hypoosmotic shock and promotes survival in the aquatic environment. Appl. Environ. Microbiol., 2018, vol. 84, no. 5: e02203-17. doi: 10.1128/AEM.02203-17
  90. Wittwer M., Altpeter E., Pilo P., Gygli S.M., Beuret C., Foucault F., Ackermann-Gaumann R., Karrer U., Jacob D., Grunow R., Schurch N. Population genomics of Francisella tularensis subsp. holarctica and its implication on the eco-epidemiology of tularemia in Switzerland. Front. Cell. Infect. Microbiol., 2018, vol. 8: 89. doi: 10.3389/fcimb.2018.00089

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