References

microbe

Проблемы особо опасных инфекций

Problems of Particularly Dangerous Infections

0370-10692658-719X

Russian Research Anti-Plague Institute “Microbe”

10.21055/0370-1069-2021-3-23-32

microbe-1544

Research Article

ОБЗОРЫ

REVIEWS

Пути распространения сибирской язвы в природных экосистемах

Routes of Spread of Anthrax in Natural Ecosystems

https://orcid.org/0000-0002-9501-1380

Тимофеев

В. С.

Timofeev

V. S.

142279, Московская обл., п. Оболенск

Obolensk, Moscow Region, Russian Federation, 142279

timofeev_vitalii@mail.ru

https://orcid.org/0000-0002-6897-3613

Бахтеева

И. В.

Bakhteeva

I. V.

142279, Московская обл., п. Оболенск

Obolensk, Moscow Region, Russian Federation, 142279

https://orcid.org/0000-0001-9478-5563

Титарева

Г. М.

Titareva

G. M.

142279, Московская обл., п. Оболенск

Obolensk, Moscow Region, Russian Federation, 142279

https://orcid.org/0000-0003-1682-8788

Гончарова

Ю. О.

Goncharova

Yu. O.

142279, Московская обл., п. Оболенск

Obolensk, Moscow Region, Russian Federation, 142279

https://orcid.org/0000-0003-1078-4585

Дятлов

И. А.

Dyatlov

I. A.

142279, Московская обл., п. Оболенск

Obolensk, Moscow Region, Russian Federation, 142279

ФБУН «Государственный научный центр прикладной микробиологии и биотехнологии»РоссияState Scientific Center of Applied Microbiology and BiotechnologyRussian Federation

2021

22102021

032332

2021

Тимофеев В.С., Бахтеева И.В., Титарева Г.М., Гончарова Ю.О., Дятлов И.А.

Timofeev V.S., Bakhteeva I.V., Titareva G.M., Goncharova Y.O., Dyatlov I.A.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://journal.microbe.ru/jour/article/view/1544

Сибирская язва – особо опасный зооантропоноз, вызываемый грамположительной спорообразующей бактерией Bacillus anthracis. Это заболевание поражает преимущественно копытных травоядных животных, в том числе использующихся в сельском хозяйстве, но может встречаться у других животных и человека. Именно сибиреязвенной инфекции человека и сельскохозяйственных животных посвящено большинство исследований. В то же время вопросы эпидемиологии сибирской язвы в природных экосистемах освещены в литературе недостаточно подробно и зачастую весьма фрагментарно. В данном обзоре проведен анализ литературных источников, описывающих основные пути и способы распространения различных клинических форм сибиреязвенной инфекции в природе, в первую очередь среди диких животных. В том числе мы касаемся некоторых неочевидных аспектов алиментарного заражения сибирской язвой, например, объясняющих разницу в чувствительности к заражению травоядных и хищных млекопитающих и даже разных половозрастных групп в пределах одного вида.

Anthrax is a particularly dangerous zooanthroponosis caused by the Gram-positive spore-forming bacterium Bacillus anthracis. This disease mainly affects hoofed herbivores, including those used in agriculture, but can occur in other animals and in humans. That is why the majority of studies of this infection are focused on anthrax in humans and farm animals, as the most important issues from a practical point of view. At the same time, the issues of anthrax epidemiology in natural ecosystems are described in the literature in insufficient detail and often very fragmentary. This paper provides a review of the literature describing the main pathways, patterns and risks of the spread of various clinical forms of anthrax infection in nature, primarily among wild animals. Among other things, we cover some non-notable aspects of intestinal infection with anthrax which, for instance, explain the difference in sensitivity to infection in herbivorous and carnivorous mammals and even different sex and age groups within the same species.

Bacillus anthracisсибирская язвадикие животныеэпидемиология

Bacillus anthracisanthraxwild animalsepidemiology

References1

Collier R.J. Membrane translocation by anthrax toxin. Mol. Aspects Med. 2009; 30(6):413–22. DOI: 10.1016/j.mam.2009.06.003.

Swick M.C., Koehler T.M., Driks A. Surviving between hosts: sporulation and transmission. Microbiol. Spectr. 2016; 4(4):10.1128/microbiolspec.VMBF-0029-2015. DOI: 10.1128/microbiolspec.VMBF-0029-2015.

Park J.M., Greten F.R., Li Z.W., Karin M. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science. 2002; 297(5589):2048–51. DOI: 10.1126/science.1073163.

Sharma S., Bhatnagar R., Gaur D. Bacillus anthracis poly- γ-D-glutamate capsule inhibits opsonic phagocytosis by impeding complement activation. Front. Immunol. 2020; 11:462. DOI: 10.3389/fimmu.2020.00462.

Ehling-Schulz M., Lereclus D., Koehler T.M. The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiol. Spectr. 2019; 7(3):10.1128/microbiolspec.GPP3-0032-2018. DOI: 10.1128/microbiolspec.GPP3-0032-2018.

Dragon D.C., Rennie R.P. The ecology of anthrax spores: tough but not invincible. Can. Vet. J. 1995; 36(5):295–301. PMID: 7773917; PMCID: PMC1686874.

Brawand S. G., Kittl S., Dettwiler M., Thomann A., Feyer S., Cachim J., Theubet G., Liechti N., Wittwer M., Schürch N., Oberhänsli S., Heinimann A., Jores J. An unusual case of bovine anthrax in the canton of Jura, Switzerland in 2017. BMC Vet. Res. 2019; 15(1):265. DOI: 10.1186/s12917-019-1996-4.

Timofeev V., Bahtejeva I., Mironova R., Titareva G., Lev I., Christiany D., Borzilov A., Bogun A., Vergnaud G. Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia. PLoS One. 2019; 14(5):e0209140. DOI: 10.1371/journal.pone.0209140.

Anthrax in humans and animals. 4th ed. Geneva: World Health Organization; 2008.

Finke E.J., Beyer W., Loderstädt U., Frickmann H. Review: The risk of contracting anthrax from spore-contaminated soil – A military medical perspective. Eur. J. Microbiol. Immunol. (Bp). 2020; 10(2):29–63. DOI: 10.1556/1886.2020.00008.

Ngetich W. Review of anthrax: a disease of animals and humans. Int. J. Agric. Environ. Bio-res. 2019; 4(1):123–34.

Munyua P., Bitek A., Osoro E., Pieracci E.G., Muema J., Mwatondo A., Kungu M., Nanyingi M., Gharpure R., Njenga K., Thumbi S.M. Prioritization of zoonotic diseases in Kenya, 2015. PLoS One. 2016; 11(8):e0161576. DOI: 10.1371/journal.pone.0161576.

Carlson C.J., Kracalik I.T., Ross N., Alexander K.A., HughJones M.E., Fegan M., Elkin B.T., Epp T., Shury T.K., Zhang W., Bagirova M., Getz W.M., Blackburn J.K. The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife. Nat. Microbiol. 2019; 4(8):1337–43. DOI: 10.1038/s41564-019-0435-4.

Webb G.F. A silent bomb: the risk of anthrax as a weapon of mass destruction. Proc. Natl. Acad. Sci. U S A. 2003; 100(8):4355–6. DOI: 10.1073/pnas.0830963100.

Savransky V., Ionin B., Reece J. Current status and trends in prophylaxis and management of anthrax disease. Pathogens. 2020; 9(5):370. DOI: 10.3390/pathogens9050370.

Cieslak T.J., Eitzen E.M.Jr. Clinical and epidemiologic principles of anthrax. Emerg. Infect. Dis. 1999; 5(4):552–5. DOI: 10.3201/eid0504.990418.

CDC Anthrax. [Internet]. URL: https://www.cdc.gov/anthrax/index.html (Accessed: October 10, 2019).

Zasada AA. Injectional anthrax in human: A new face of the old disease. Adv. Clin. Exp. Med. 2018; 27(4):553–8. DOI: 10.17219/acem/68380.

Carlson C.J., Getz W.M., Kausrud K.L., Cizauskas C.A., Blackburn J.K., Bustos Carrillo F.A., Colwell R., Easterday W.R., Ganz H.H., Kamath P.L., Økstad O.A., Turner W.C., Kolstø A.B., Stenseth N.C. Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis). Biol. Rev. Camb. Philos. Soc. 2018; 93(4):1813–31. DOI: 10.1111/brv.12420.

Turner W.C., Kausrud K.L., Krishnappa Y.S., Cromsigt J.P., Ganz H.H., Mapaure I., Cloete C.C., Havarua Z., Küsters M., Getz W.M., Stenseth N.C. Fatal attraction: vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites. Proc. Biol. Sci. 2014; 281(1795):20141785. DOI: 10.1098/rspb.2014.1785.

Ganz H.H., Turner W.C., Brodie E.L., Kusters M., Shi Y., Sibanda H., Torok T., Getz W.M. Interactions between Bacillus anthracis and plants may promote anthrax transmission. PLoS Negl. Trop. Dis. 2014; 8(6):e2903. DOI: 10.1371/journal.pntd.0002903.

Joly K., Gurarie E., Sorum M.S., Kaczensky P., Cameron M.D., Jakes A.F., Borg B.L., Nandintsetseg D., Hopcraft J.G.C., Buuveibaatar B., Jones P.F., Mueller T., Walzer C., Olson K.A., Payne J.C., Yadamsuren A., Hebblewhite M. Longest terrestrial migrations and movements around the world. Sci. Rep. 2019; 9(1):15333. DOI: 10.1038/s41598-019-51884-5.

Cizauskas C.A., Bellan S.E., Turner W.C., Vance R.E., Getz W.M. Frequent and seasonally variable sublethal anthrax infections are accompanied by short-lived immunity in an endemic system. J. Anim. Ecol. 2014; 83(5):1078–90. DOI: 10.1111/1365-2656.12207.

Fox M.D., Boyce J.M., Kaufmann A.F., Young J.B., Whitford H.W. An epizootiologic study of anthrax in Falls County, Texas. J. Am. Vet. Med. Assoc. 1977; 170(3):327–33. PMID: 401803.

Turner W.C., Kausrud K.L., Beyer W., Easterday W.R., Barandongo Z.R., Blaschke E., Cloete C.C., Lazak J., Van Ert M.N., Ganz H.H., Turnbull P.C., Stenseth N.C., Getz W.M. Lethal exposure: An integrated approach to pathogen transmission via environmental reservoirs. Sci. Rep. 2016; 6:27311. DOI: 10.1038/srep27311.

Hanna P.C., Ireland J.A. Understanding Bacillus anthracis pathogenesis. Trends Microbiol. 1999; 7(5):180–2. DOI: 10.1016/s0966-842x(99)01507-3.

Frederick R.S., Ernest T.T., David R.F. Medical aspects of chemical and biological warfare. Washington: Office of the Surgeon General, Borden Institute, Walter Reed Army Medical Center; 1997. Р. 467–478.

Xie T., Sun C., Uslu K., Auth R.D., Fang H., Ouyang W., Frucht D.M. A new murine model for gastrointestinal anthrax infection. PLoS One. 2013; 8(6):e66943. DOI: 10.1371/journal.pone.0066943.

Bishop B.L., Lodolce J.P., Kolodziej L.E., Boone D.L., Tang W.J. The role of anthrolysin O in gut epithelial barrier disruption during Bacillus anthracis infection. Biochem. Biophys. Res. Commun. 2010; 394(2):254–9. DOI: 10.1016/j.bbrc.2010.02.091.

Hugh-Jones M., Blackburn J. The ecology of Bacillus anthracis. Mol. Aspects Med. 2009; 30(6):356–67. DOI: 10.1016/j.mam.2009.08.003.

Hugh-Jones M.E., de Vos V. Anthrax and wildlife. Rev. Sci. Tech. 2002; 21(2):359–83. DOI: 10.20506/rst.21.2.1336.

Hampson K., Lembo T., Bessell P., Auty H., Packer C., Halliday J., Beesley C.A., Fyumagwa R., Hoare R., Ernest E., Mentzel C., Metzger K.L., Mlengeya T., Stamey K., Roberts K., Wilkins P.P., Cleaveland S. Predictability of anthrax infection in the Serengeti, Tanzania. J. Appl. Ecol. 2011; 48(6):1333–44. DOI: 10.1111/j.1365-2664.2011.02030.x.

Appleby J.C. The isolation and classification of proteolytic bacteria from the rumen of the sheep. J. Gen. Microbiol. 1955; 12(3):526–33. DOI: 10.1099/00221287-12-3-526.

Fox M.D., Kaufmann A.F., Zendel S.A., Kolb R.C., Songy Jr. C.G., Cangelosi D.A., Fuller C.E. Anthrax in Louisiana, 1971: epizootiologic study. J. Am. Vet. Med. Assoc. 1973; 163(5):446–51.

Gates C.C., Elkin B.T., Dragon D.C. Investigation, control and epizootiology of anthrax in a geographically isolated, freeroaming bison population in northern Canada. Can. J. Vet. Res. 1995; 59(4):256–64.

Ruckstuhl K.E. Sexual segregation in vertebrates: proximate and ultimate causes. Integr. Comp. Biol. 2007; 47(2):245–57. DOI: 10.1093/icb/icm030.

Lindeque P.M., Turnbull P.C. Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort J. Vet. Res. 1994;61(1):71–83.

Barboza P.S., Bowyer T.R. Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J. Mammalogy. 2000; 81(2):473–89. DOI: 10.1644/1545-1542(2000)081<0473:SSIDDA>2.0.CO;2.

Yang A., Proffitt K.M., Asher V., Ryan S.J., Blackburn J.K. Sex-specific elk resource selection during the anthrax risk period. J. Wildl. Manag. 2020; 84(7):1–11. DOI: 10.1002/jwmg.21952.

Diao Q., Zhang R., Fu T. Review of strategies to promote rumen development in calves. Animals (Basel). 2019; 9(8):490. DOI: 10.3390/ani9080490.

Glomski I.J., Piris-Gimenez A., Huerre M., Mock M., Goossens P.L. Primary involvement of pharynx and peyer’s patch in inhalational and intestinal anthrax. PLoS Pathog. 2007; 3(6):e76. DOI: 10.1371/journal.ppat.0030076.

Coleman M.E., Thran B., Morse S.S., Hugh-Jones M., Massulik S. Inhalation anthrax: dose response and risk analysis. Biosecur. Bioterror. 2008; 6(2):147–60. DOI: 10.1089/bsp.2007.0066.

Druette H.A., Henderson D.W., Packman L., Peacock S. Studies on respiratory infection. I. The influence of particle size on respiratory infection with anthrax spores. J. Hyg. (Lond). 1953; 51(3):359–71. DOI: 10.1017/s0022172400015795.

Schelkle B., Choi Y., Baillie L.W., Richter W., Buyuk F., Celik E., Wendling M., Sahin M., Gallagher T. Caenorhabditis elegans predation on Bacillus anthracis: Decontamination of spore contaminated soil with germinants and nematodes. Front. Microbiol. 2018; 8:2601. DOI: 10.3389/fmicb.2017.02601.

Dragon D.C., Rennie R.P., Elkin B.T. Detection of anthrax spores in endemic regions of northern Canada. J. Appl. Microbiol. 2001; 91(3):435–41. DOI: 10.1046/j.1365-2672.2001.01389.x.

Curie M. Anthrax environmental decontamination network. [Internet]. URL: https://aednetproject.wordpress.com (Accessed: October 20, 2019).

Turnbull P.C., Lindeque P.M., Le Roux J., Bennett A.M., Parks S.R. Airborne movement of anthrax spores from carcass sites in the Etosha National Park, Namibia. J. Appl. Microbiol. 1998; 84(4):667–76. DOI: 10.1046/j.1365-2672.1998.00394.x.

Peters C.J., Hartley D.M. Anthrax inhalation and lethal human infection. Lancet. 2002; 359(9307):710–1. DOI: 10.1016/s0140-6736(02)07792-9.

Barandongo Z.R., Mfune J.K.E., Turner W.C. Dust-bathing behaviors of African herbivores and the potential risk of inhalational anthrax. J. Wildl. Dis. 2018; 54:34–44. DOI: 10.7589/2017-04-069.

Brachman P.S., Kaufman A.F., Dalldorf F.G. Industrial inhalation Anthrax. Bacteriol. Rev. 1966; 30(3):646–59. DOI: 10.1128/br.30.3.646-659.1966.

D’Amelio E., Gentile B., Lista F., D’Amelio R. Historical evolution of human anthrax from occupational disease to potentially global threat as bioweapon. Environ. Int. 2015; 85: 133–46. DOI: 10.1016/j.envint.2015.09.009.

Kraneveld F.C., Mansjoer M. Anthrax bacilli in the digestive tract of Tabanus rubidus. Nederlands-indische Bladen Voor Diergeneeskunde. 1939: 51:62–75.

Kraneveld F.C., Djaenodin M. Test on the dissemination of anthrax by Tabanus rubidus, in horses and buffalo. Nederlandsindische Bladen Voor Diergeneeskunde. 1940; 52: 339–80.

Blackburn J.K. Evaluating the spatial ecology of anthrax in North America: examining epidemiological components across multiple geographic scales using a GIS-based approach: doctoral dissertation. LA: Louisiana State University; 2006. 141 p.

Turell M.J., Knudson G.B. Mechanical transmission of Bacillus anthracis by stable flies (Stomoxys calcitrans) and mosquitoes (Aedes aegypti and Aedes taeniorhynchus). Infect. Immun. 1987; 55(8):1859–61. DOI: 10.1128/IAI.55.8.1859-1861.1987.

Morris H. Blood-sucking insects as transmitters of anthrax or charbon. LSU Agricultural Experiment Station Reports 1918. [Internet]. URL: http://digitalcommons.lsu.edu/agexp/302 (Accessed: October 22, 2019).

Braack L.E., De Vos V. Feeding habits and flight range of blow-flies (Chrysomyia spp.) in relation to anthrax transmission in the Kruger National Park, South Africa. Onderstepoort. J. Vet. Res. 1990; 57(2):141–2.

Fasanella A., Scasciamacchia S., Garofolo G., Giangaspero A., Tarsitano E., Adone R. Evaluation of the house fly Musca domestica as a mechanical vector for an anthrax. PLoS One. 2010; 5(8):e12219. DOI: 10.1371/journal.pone.0012219.

Grunow R., Verbeek L., Jacob D., Holzmann T., Birkenfeld G., Wiens D., von Eichel-Streiber L., Grass G., Reischl U. Injection anthrax – a new outbreak in heroin users. Dtsch. Arztebl. Int. 2012; 109(49):843–8. DOI: 10.3238/arztebl.2012.0843.

Russell L., Pedersen M., Jensen A.V., Søes L.M., Hansen A.B. Two anthrax cases with soft tissue infection, severe oedema and sepsis in Danish heroin users. BMC Infect. Dis. 2013; 13:408. DOI: 10.1186/1471-2334-13-408.

Hanczaruk M., Reischl U., Holzmann T., Frangoulidis D., Wagner D.M., Keim P.S., Antwerpen M.H., Meyer H., Grass G. Injectional anthrax in heroin users, Europe, 2000–2012. Emerg. Infect. Dis. 2014; 20(2):322–3. DOI: 10.3201/eid2002.120921.

Van Ert M.N., Easterday W.R., Huynh L.Y., Okinaka R.T., Hugh-Jones M.E., Ravel J., Zanecki S.R., Pearson T., Simonson T.S., U’Ren J.M., Kachur S.M., Leadem-Dougherty R.R., Rhoton S.D., Zinser G., Farlow J., Coker P.R., Smith K.L., Wang B., Kenefic L.J., Fraser-Liggett C.M., Wagner D.M., Keim P. Global genetic population structure of Bacillus anthracis. PLoS One. 2007; 2(5):e461. DOI: 10.1371/journal.pone.0000461.

Kolstø A.B., Tourasse N.J., Økstad O.A. What sets Bacillus anthracis apart from other Bacillus species? Annu. Rev. Microbiol. 2009; 63:451–76. DOI: 10.1146/annurev.micro.091208.073255.

Vergnaud G. Bacillus Anthracis evolutionary history: taking advantage of the topology of the phylogenetic tree and of human history to propose dating points. Erciyes. Med. J. 2020; 42(4):362–9. DOI: 10.14744/etd.2020.64920.

The authors declare that there are no conflicts of interest present.