Environmental suitability of Yersinia pestis and the spatial dynamics of plague in the Qinghai Lake region, China


Arotolu TE, Wang HN, Lv JN, Kun S, Huang LY, Wang XL (2022): Environmental suitability of Yersinia pestis and the spatial dynamics of plague in the Qinghai Lake region, China. Vet Med-Czech 67, 569–578.

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Plague, a highly infectious disease caused by Yersinia pestis, has killed millions of people in history and is still active in the natural foci of the world nowadays. Understanding the spatiotemporal patterns of plague outbreaks in history is critically important, as it may help facilitate the prevention and control for potential future outbreaks. This study’s objective was to estimate the effect of the topography, vegetation, climate, and other environmental factors on the Y. pestis ecological niche. A maximum entropy algorithm spatially modelled plague occurrence data from 2004–2018 and the environmental variables to evaluate the contribution of the variables to the distribution of Y. pestis. Our results found that the average minimum temperature in September (–8 °C to +5 °C) and the sheep population density (250 sheep per km2) were influential in characterising the niche. The rim of Qinghai Lake showed more favourable conditions for Y. pestis presence than other areas within the study area. Identifying various factors will assist any future modelling efforts. Our suitability map identifies hotspots and will help public health officials in resource allocation in their quest to abate future plague outbreaks.

Aiello-Lammens ME, Boria RA, Radosavljevic A, Vilela B, Anderson RP. spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography. 2015 Feb;38(5):541-5.
Assefa A, Tibebu A, Bihon A, Yimana M. Global ecological niche modelling of current and future distribution of peste des petits ruminants virus (PPRv) with an ensemble modelling algorithm. Transbound Emerg Dis. 2021 Nov;68(6):3601-10. https://doi.org/10.1111/tbed.13967
CNR – China National Radio. Pneumonic plague kills two, infects 10 in Qinghai [Internet]. 2009 [cited 2021 Mar 19]. Available from covid-19.chinadaily.com.cn/china/2009-08/03/content_8510436.htm.
Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully Jr JF, Gage KL, Kosoy MY, Loye JE, Martin AP. Testing the generality of a trophic-cascade model for plague. EcoHealth. 2005 May;2(2):102-12.
Dubyanskiy VM, Yeszhanov AB. Ecology of Yersinia pestis and the epidemiology of plague. In: Yang R, Anisimov A, editors. Yersinia pestis: Retrospective and perspective. Dordrecht: Springer Netherlands; 2016. p. 101-70.
Duplantier JM, Duchemin JB, Chanteau S, Carniel E. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res. 2005 May-Jun;36(3):437-53. https://doi.org/10.1051/vetres:2005007
Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JMcC, Townsend Peterson A, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE. Novel methods improve prediction of species’ distributions from occurrence data. Ecography. 2006 Mar;29(2):129-51. https://doi.org/10.1111/j.2006.0906-7590.04596.x
Gage KL, Burkot TR, Eisen RJ, Hayes EB. Climate and vectorborne diseases. Am J Prev Med. 2008 Nov;35(5):436-50.
Gage KL, Kosoy MY. Natural history of plague: Perspectives from more than a century of research. Annu Rev Entomol. 2005;50:505-28. https://doi.org/10.1146/annurev.ento.50.071803.130337
Gao S, Zeng Z, Wang H, Chen F, Huang L, Wang X. Predicting the possibility of African horse sickness (AHS) introduction into China using spatial risk analysis and habitat connectivity of Culicoides. Sci Rep. 2022 Mar 10;12(1):3910.
Goldberg AR, Conway CJ, Biggins DE. Flea sharing among sympatric rodent hosts: Implications for potential plague effects on a threatened sciurid. Ecosphere. 2020 Feb;11(2):e03033. https://doi.org/10.1002/ecs2.3033
Gong J, Li J, Yang J, Li S, Tang W. Land use and land cover change in the Qinghai Lake region of the Tibetan plateau and its impact on ecosystem services. Int J Environ Res Public Health. 2017 Jul 21;14(7):818. https://doi.org/10.3390/ijerph14070818
Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982 Apr;143(1):29-36. https://doi.org/10.1148/radiology.143.1.7063747
Heikkinen RK, Luoto M, Araujo MB, Virkkala R, Thuiller W. Sykes MT. Methods and uncertainties in bioclimatic envelope modelling under climate change. Prog Phys Geogr. 2006;30(6):751-77. https://doi.org/10.1177/0309133306071957
Hinnebusch BJ, Fischer ER, Schwan TG. Evaluation of the role of the Yersinia pestis plasminogen activator and other plasmid-encoded factors in temperature-dependent blockage of the flea. J Infect Dis. 1998 Nov;178(5):1406-15. https://doi.org/10.1086/314456
Hueffer K, Drown D, Romanovsky V, Hennessy T. Factors contributing to anthrax outbreaks in the circumpolar North. Ecohealth. 2020 Mar;17(1):174-80. https://doi.org/10.1007/s10393-020-01474-z
Jacome G, Vilela P, Yoo C. Social-ecological modelling of the spatial distribution of dengue fever and its temporal dynamics in Guayaquil, Ecuador for climate change adaption. Ecol Inform. 2019 Jan;49:1-12. https://doi.org/10.1016/j.ecoinf.2018.11.001
Ji S. [Plague]. Beijing, China: People’s Medical Publishing House; 1988. Chinese.
Latham J, Cumani R, Rosati I, Bloise M. Global land cover share (GLC-SHARE) database beta-release version 1.0-2014. Rome, Italy: FAO; 2014. 40 p.
Li Y, Dong S, Liu S, Zhou H, Gao Q, Cao G, Wang X, Su X, Zhang Y, Tang L, Zhao H, Wu X. Seasonal changes of CO2, CH4 and N2O fluxes in different types of alpine grassland in the Qinghai-Tibetan plateau of China. Soil Biol Biochem. 2015 Jan;80:306-14. https://doi.org/10.1016/j.soilbio.2014.10.026
Li YF, Li DB, Shao HS, Li HJ, Han YD. Plague in China 2014 – All sporadic case report of pneumonic plague. BMC Infect Dis. 2016 Feb 19;16:85. https://doi.org/10.1186/s12879-016-1403-8
Lu L, Ren Z, Yue Y, Yu X, Lu S, Li G, Li H, Wei J, Liu J, Mu Y, Hai R, Yang Y, Wei R, Kan B, Wang H, Wang J, Wang Z, Liu Q, Xu J. Niche modeling predictions of the potential distribution of Marmota himalayana, the host animal of plague in Yushu county of Qinghai. BMC Public Health. 2016 Feb 24;16:183. https://doi.org/10.1186/s12889-016-2697-6
Miller D. The importance of China’s nomads. Rangel Arch. 2002 Feb;24(1):22-4. https://doi.org/10.2458/azu_rangelands_v24i1_miller
Nyirenda SS, Hang’ombe BM, Machang’u R, Mwanza J, Kilonzo BS. Identification of risk factors associated with transmission of plague disease in eastern Zambia. Am J Trop Med Hyg. 2017 Sep;97(3):826-30. https://doi.org/10.4269/ajtmh.16-0990
Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL. Incidence of plague associated with increased winter-spring precipitation in New Mexico. Am J Trop Med Hyg. 1999 Nov;61(5):814-21.
Pearson R, Raxworthy C, Nakamura M, Peterson AT. Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar. J Biogeogr. 2007 Jan;34(1):102-17. https://doi.org/10.1111/j.1365-2699.2006.01594.x
Peterson AT, Papes M, Eaton M. Transferability and model evaluation in ecological niche modeling: A comparison of GARP and Maxent. Ecography. 2007 Aug;30(4):550-60.
Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecol Model. 2006 Jan;190(3-4):231-59. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Phillips SJ, Dudik M. Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography. 2008 Mar;31(2):161-75. https://doi.org/10.1111/j.0906-7590.2008.5203.x
Qian Q, Zhao J, Fang L, Zhou H, Zhang W, Wei L, Yang H, Yin W, Cao W, Li Q. Mapping risk of plague in Qinghai-Tibetan plateau, China. BMC Infect Dis. 2014 Jul 10;14:382.
Shi SM, Liu FY, Yan XB. [Habitat selection by Marmota himalayana in the eastern Qilian mountains]. J Gansu Agr Uni. 2008 Feb,43:125-30. Chinese.
Skowronek S, Van De Kerchove R, Rombouts B, Aerts R, Ewald M, Warrie J, Schiefer F, Garzon-Lopez C, Hattab T, Honnay O, Lenoir J, Rocchini D, Schmidtlein S, Somers B, Feilhauer H. Transferability of species distribution models for the detection of an invasive alien bryophyte using imaging spectroscopy data. Int J Appl Earth Obs Geoinf. 2018 Feb;68:61-72.
Stapp P, Antolin MF, Ball M. Patterns of extinction in prairie dog metapopulations: Plague outbreaks follow El Nino events. Front Ecol Environ. 2004 Jun;2(5):235-40. https://doi.org/10.1890/1540-9295(2004)002[0235:POEIPD]2.0.CO;2
Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L. Plague: Past, present, and future. PLoS Med. 2008 Jan 15;5(1):e3. https://doi.org/10.1371/journal.pmed.0050003
Tian F. [Investigation of the nature focus of Marmota himalayana]. Chin J Zoonoses. 2000;16(4):95-7. Chinese.
Wang H, Cui Y, Wang Z, Wang X, Guo Z, Yan Y, Li C, Cui B, Xiao X, Yang Y, Qi Z, Wang G, Wei B, Yu S, He D, Chen H, Chen G, Song Y, Yang R. A dog-associated primary pneumonic plague in Qinghai province, China. Clin Infect Dis. 2011 Jan 15;52(2):185-90.
Wang ZY, Cui B, Qi Z, Chen H, Wei R. [Plague in Qinghai]. Beijing: People’s Medical Publishing House; 2016. Chinese.
Wang ZY. [The control policy of Tibetan sheep plague in Qinghai]. Chin J Zoonoses. 1999 Jan;15(6):95-106. Chinese.
Werner SB, Weidmer CE, Nelson BC, Nygaard GS, Goethals RM, Poland JD. Primary plague pneumonia contracted from a domestic cat at South Lake Tahoe, Calif. JAMA. 1984 Feb 17;251(7):929-31.
WHO – World Health Organization. Plague [Internet]. 2004 [cited 2021 Mar 19]. Available from www.who.int/csr/disease/plague/en/.
Wong D, Wild MA, Walburger MA, Higgins CL, Callahan M, Czarnecki LA, Lawaczeck EW, Levy CE, Patterson JG, Sunenshine R, Adem P, Paddock CD, Zaki SR, Petersen JM, Schriefer ME, Eisen RJ, Gage KL, Griffith KS, Weber IB, Spraker TR, Mead PS. Primary pneumonic plague contracted from a mountain lion carcass. Clin Infect Dis. 2009 Aug 1;49(3):e33-8. https://doi.org/10.1086/600818
Xinhua. Bubonic plague kills 8 in northwest China [Internet]. 2004 [cited 2021 Apr 26]. Available from: www.chinadaily.com.cn/english/doc/2004-10/28/content_386485.htm.
Xinhua. One plague case reported in Inner Mongolia [Internet]. 2019a [cited 2021 May 28]. Available from: edition.cnn.com/2020/07/06/asia/china-mongolia-bubonic-plague-intl-hnk-scli-scn/index.html.
Xinhua. Two people just got the plague in China — yes, the Black Death plagues [Internet]. 2019b [cited 2021 May 30]. Available from www.xinhuanet. com/english/2019-11/17/c_138562299.htm.
Xu X, Cui Y, Xin Y, Yang X, Zhang Q, Jin Y, Zhao H, He J, Jin X, Li C, Jin J, Li X, Wu H, Qi Z. Genetic diversity and spatial-temporal distribution of Yersinia pestis in Qinghai plateau, China. PLoS Negl Trop Dis. 2018 Jun 25;12(6):e0006579. https://doi.org/10.1371/journal.pntd.0006579
Zeng Z, Gao S, Wang HN, Huang LY, Wang XL. A predictive analysis on the risk of peste des petits ruminants in livestock in the Trans-Himalayan region and validation of its transboundary transmission paths. PLoS One. 2021 Sep 10;16(9):e0257094.
Zhao J, Xu M, Lu SL, Cao CX. Human settlement evaluation in mountain areas based on remote sensing, GIS and ecological niche modeling. J Mt Sci. 2013 May;10(3):378-87. https://doi.org/10.1007/s11629-013-2413-2
Zietz BP, Dunkelberg H. The history of the plague and the research on the causative agent Yersinia pestis. Int J Hyg Environ Health. 2004 Feb;207(2):165-78. https://doi.org/10.1078/1438-4639-00259
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