Top

Published in:

Open Access 01-12-2018 | Research article

Landscape and rodent community composition are associated with risk of hemorrhagic fever with renal syndrome in two cities in China, 2006–2013

Authors: Hong Xiao, Xin Tong, Ru Huang, Lidong Gao, Shixiong Hu, Yapin Li, Hongwei Gao, Pai Zheng, Huisuo Yang, Zheng Y. X. Huang, Hua Tan, Huaiyu Tian

Published in: BMC Infectious Diseases | Issue 1/2018

Abstract

Background

Hemorrhagic fever with renal syndrome (HFRS) is a rodent-borne disease caused by hantaviruses. Landscape can influence the risk of hantavirus infection for humans, mainly through its effect on rodent community composition and distribution. It is important to understand how landscapes influence population dynamics for different rodent species and the subsequent effect on HFRS risk.

Methods

To determine how rodent community composition influenced human hantavirus infection, we monitored rodent communities in the prefecture-level cities of Loudi and Shaoyang, China, from 2006 to 2013. Land use data were extracted from satellite images and rodent community diversity was analyzed in 45 trapping sites, in different environments. Potential contact matrices, determining how rodent community composition influence HFRS infection among different land use types, were estimated based on rodent community composition and environment type for geo-located HFRS cases.

Results

Apodemus agrarius and Rattus norvegicus were the predominant species in Loudi and Shaoyang, respectively. The major risk of HFRS infection was concentrated in areas with cultivated land and was associated with A. agrarius, R. norvegicus, and Rattus flavipectus. In urban areas in Shaoyang, Mus musculus was related to risk of hantavirus infection.

Conclusions

Landscape features and rodent community dynamics may affect the risk of human hantavirus infection. Results of this study may be useful for the development of HFRS prevention initiatives that are customized for regions with different geographical environments.

Clement J, Maes P, Lagrou K, Van Ranst M, Lameire N. A unifying hypothesis and a single name for a complex globally emerging infection: hantavirus diseases. Eur J Clin Microbiol Infect Dis. 2012;31(1):1–5.CrossRefPubMed

Huang XX, Yin HM, Yan L, Wang XF, Wang SW. Epidemiologic characteristics of haemorrhagic fever with renal syndrome in mainland China from 2006 to 2010. West Pac Surveill Response J. 2012;3(1):12–8.

Hansen A, Cameron S, Liu Q, Sun Y, Weinstein P, Williams C, Han G-S, Bi P. Transmission of haemorrhagic fever with renal syndrome in China and the role of climate factors: a review. Int J Infect Dis. 2015;33:212–8.CrossRefPubMed

Xiao H, Tian HY, Cazelles B, Li XJ, Tong SL, Gao LD, Qin JX, Lin XL, Liu HN, Zhang XX. Atmospheric moisture variability and transmission of hemorrhagic fever with renal syndrome in Changsha City, mainland China, 1991-2010. PLoS Negl Trop Dis. 2013;7(6):e2260.CrossRefPubMedPubMedCentral

Fang LQ, Wang XJ, Liang S, Li YL, Song SX, Zhang WY, Qian Q, Li YP, Wei L, Wang ZQ, et al. Spatiotemporal trends and climatic factors of hemorrhagic fever with renal syndrome epidemic in Shandong Province, China. PLoS Negl Trop Dis. 2010;4(8):e789.CrossRefPubMedPubMedCentral

Yan L, Fang LQ, Huang HG, Zhang LQ, Feng D, Zhao WJ, Zhang WY, Li XW, Cao WC. Landscape elements and hantaan virus-related hemorrhagic fever with renal syndrome, People's Republic of China. Emerg Infect Dis. 2007;13(9):1301–6.CrossRefPubMedPubMedCentral

Tian H, Yu P, Cazelles B, Xu L, Tan H, Yang J, Huang S, Xu B, Cai J, Ma C. Interannual cycles of Hantaan virus outbreaks at the human–animal interface in Central China are controlled by temperature and rainfall. Proceedings of the National Academy of Sciences 2017:201701777.

Liu X, Jiang B, Bi P, Yang W, Liu Q. Prevalence of haemorrhagic fever with renal syndrome in mainland China: analysis of National Surveillance Data, 2004-2009. Epidemiol Infect. 2012;140(5):851–7.CrossRefPubMed

Xiao H, Tian HY, Dai XY, Lin XL, Zhu PJ, Gao LD, Chen BY, Zhang XX. Study on the influence of elements regrading on the transmission of hemorrhagic fever with renal syndrome in Changsha [in Chinese]. Chin J Pre Med. 2012;46(3):246–51.

10.

Liu HN, Gao LD, Chowell G, Hu SX, Lin XL, Li XJ, Ma GH, Huang R, Yang HS, Tian HY, et al. Time-specific ecologic niche models forecast the risk of hemorrhagic fever with renal syndrome in Dongting Lake district, China, 2005-2010. PLoS One. 2014;9(9):e106839.CrossRefPubMedPubMedCentral

11.

Xiao H, Lin XL, Gao LD, Dai XY, He XG, Chen BY, Zhang XX, Zhao J, Tian HY. Environmental factors contributing to the spread of hemorrhagic fever with renal syndrome and potential risk areas prediction in midstream and downstream of the Xiangjiang River [in Chinese]. Sci Geogr Sin. 2013;33(1):123–8.

12.

Liu FQ, Gao LD, Dai DF, Zhang H, Zeng G, Guo SH, Wu ZG, Hu SX. Study on hemorrhagic fever with renal syndrome surveillance in HunanProvince, 2006 [in Chinese]. Chin Prev Med. 2008;9(6):496–9.

13.

Xiao H, Tian HY, Gao LD, Liu HN, Duan LS, Basta N, Cazelles B, Li XJ, Lin XL, Wu HW, et al. Animal reservoir, natural and socioeconomic variations and the transmission of hemorrhagic fever with renal syndrome in Chenzhou, China, 2006-2010. PLoS Negl Trop Dis. 2014;8(1):e2615.CrossRefPubMedPubMedCentral

14.

Fang LZ, Zhao L, Wen HL, Zhang ZT, Liu JW, He ST, Xue ZF, Ma DQ, Zhang XS, Zhang Y, et al. Reservoir host expansion of hantavirus, China. Emerg Infect Dis. 2015;21(1):170–1.CrossRefPubMedPubMedCentral

15.

Fang LZ, Zhao L, Wen H, Zhang Z, Liu J, He S, Xue Z, Ma D, Zhang X, Zhang Y. Reservoir host expansion of hantavirus, China. Emerg Infect Dis. 2015;21(1):170.CrossRefPubMedPubMedCentral

16.

Clay CA, Lehmer EM, St Jeor S, Dearing MD. Testing mechanisms of the dilution effect: deer mice encounter rates, sin Nombre virus prevalence and species diversity. EcoHealth. 2009;6(2):250–9.CrossRefPubMed

17.

Kallio ER, Begon M, Henttonen H, Koskela E, Mappes T, Vaheri A, Vapalahti O. Cyclic hantavirus epidemics in humans--predicted by rodent host dynamics. Epidemics. 2009;1(2):101–7.CrossRefPubMed

18.

Mills JN. Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity. 2006;7(1):9–17.CrossRef

19.

Niklasson BS, Hornfeldt B, Lundkvist A, Bjorsten B, Duc JL. Temporal dynamics of Puumala virus antibody prevalence in voles and of nephropathia epidemica incidence in humans. Am J Trop Med Hyg. 1995;53(2):134–40.CrossRefPubMed

20.

Olsson GE, Hjertqvist M, Lundkvist Å, Hörnfeldt B. Predicting high risk for human hantavirus infections, Sweden. Emerg Infect Dis. 2009;15(1):104–6.CrossRefPubMedPubMedCentral

21.

Tian HY, Yu PB, Luis AD, Bi P, Cazelles B, Huang SQ, Ma CF, Zhou S, Wei J, Li S, et al. Changes in rodent abundance and weather conditions potentially drive hemorrhagic fever with renal syndrome outbreaks in Xi'an, China, 2005-2012. PLoS Ngelect Trop D. 2015;9(3):e0003530.CrossRef

22.

Wolfe ND, Daszak P, Kilpatrick AM, Burke DS. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerg Infect Dis. 2005;11(12):1822–7.CrossRefPubMedPubMedCentral

23.

Olsson GE, White N, Ahlm C, Elgh F, Verlemyr AC, Juto P, Palo RT. Demographic factors associated with hantavirus infection in bank voles (Clethrionomys Glareolus). Emerg Infect Dis. 2002;8(9):924–9.CrossRefPubMedPubMedCentral

24.

Wei L, Qian Q, Wang ZQ, Glass GE, Song SX, Zhang WY, Li XJ, Yang H, Wang XJ, Fang LQ, et al. Using geographic information system-based ecologic niche models to forecast the risk of hantavirus infection in Shandong Province, China. Am J Trop Med Hyg. 2011;84(3):497–503.CrossRefPubMedPubMedCentral

25.

Ma H, Chen H, Liu X, Guo X. Relationship between rodent population distribution and risks of major rodent-borne diseases in Nanchang. Zhongguo Meijie Shengwuxue ji Kongzhi Zazhi. 2010;21(5):450–3.

26.

Olsson GE, Leirs H, Henttonen H. Hantaviruses and their hosts in Europe: reservoirs here and there, but not everywhere? Vector Borne Zoonotic Dis. 2010;10(6):549–61.CrossRefPubMed

27.

Liu FQ, Gao LD, Dai DF, Zhang H, Hu SX, Liu YZ. Surveillance analysis of human hemorrhagic fever with renal syndrome in Hunan from 2002 to 2005 [in Chinese ]. Dis Surveillance. 2007;22(7):452–5.

28.

Ministry of Health. Handbook of epidemic hemorrhagic fever prevention and control. Beijing: China People's Health Publishing House; 1998.

29.

Xiao H, Huang R, Gao LD, Huang CR, Lin XL, Li N, Liu HN, Tong SL, Tian HY. Effects of humidity variation on the hantavirus infection and hemorrhagic fever with renal syndrome occurrence in subtropical China. Am J Trop Med Hyg. 2016;94(3):420–7.CrossRefPubMedPubMedCentral

30.

GlobCover Land Cover Maps. http://due.esrin.esa.int/page_globcover.php.

31.

Heyman P, Thoma BR, Marié JL, Cochez C, Essbauer SS. In search for factors that drive hantavirus epidemics. Front Physiol. 2012;3:237.CrossRefPubMedPubMedCentral

32.

Salkeld DJ, Padgett KA, Jones JH. A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett. 2013;16(5):679–86.CrossRefPubMed

33.

Bi P, Parton KA, Tong SL. El Nino–southern oscillation and vector-borne diseases in Anhui, China. Vector-Boren Zoonot. 2005;5(2):95–100.CrossRef

34.

Bi P, Tong SL, Donald K, Parton KA, Ni JF. Climatic, reservoir and occupational variables and the transmission of haemorrhagic fever with renal syndrome in China. Int J Epidemiol. 2002;31(1):189–93.CrossRefPubMed

35.

Zhang S, Wang S, Yin W, Liang M, Li J, Zhang Q, Feng Z, Li D. Epidemic characteristics of hemorrhagic fever with renal syndrome in China, 2006-2012. BMC Infect Dis. 2014;14:384.CrossRefPubMedPubMedCentral

36.

Hansen A, Cameron S, Liu QY, Sun YH, Weinstein P, Williams C, Han GS, Bi P. Transmission of haemorrhagic fever with renal syndrome in China and the role of climate factors: a review. Int J Infect Dis. 2015;33:212–8.CrossRefPubMed

37.

Dearing MD, Dizney L. Ecology of hantavirus in a changing world. Ann N Y Acad Sci. 2010;1195:99–112.CrossRefPubMed

Title: Landscape and rodent community composition are associated with risk of hemorrhagic fever with renal syndrome in two cities in China, 2006–2013
Authors: Hong Xiao
Xin Tong
Ru Huang
Lidong Gao
Shixiong Hu
Yapin Li
Hongwei Gao
Pai Zheng
Huisuo Yang
Zheng Y. X. Huang
Hua Tan
Huaiyu Tian
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-017-2827-5

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Landscape and rodent community composition are associated with risk of hemorrhagic fever with renal syndrome in two cities in China, 2006–2013

Abstract

Background

Methods

Results

Conclusions

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2018

Prediction of mortality in severe dengue cases

Risk factors and molecular features of sequence type (ST) 131 extended-Spectrum-β-lactamase-producing Escherichia coli in community-onset female genital tract infections

AIDS-related opportunistic illnesses and early initiation of HIV care remain critical in the contemporary HAART era: a retrospective cohort study in Taiwan

Rapid detection of respiratory organisms with the FilmArray respiratory panel in a large children’s hospital in China

Concordance of gonorrhoea of the rectum, pharynx and urethra in same-sex male partnerships attending a sexual health service in Melbourne, Australia

The systematic development of a complex intervention: HealthMap, an online self-management support program for people with HIV

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page