Skip to main content

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
Cancel
×
×
Home
  • Home
Article
  • Cited by 78
  • Cited by
    Crossref Citations
    Crossref logo
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.
    Vacchiano, Giorgio Ascoli, Davide Berzaghi, Fabio Lucas-Borja, Manuel Esteban Caignard, Thomas Collalti, Alessio Mairota, Paola Palaghianu, Ciprian Reyer, Christopher P.O. Sanders, Tanja G.M. Schermer, Eliane Wohlgemuth, Thomas and Hacket-Pain, Andrew 2018. Reproducing reproduction: How to simulate mast seeding in forest models. Ecological Modelling, Vol. 376, Issue. , p. 40.
    Guterres, Alexandro and de Lemos, Elba Regina Sampaio 2018. Hantaviruses and a neglected environmental determinant. One Health, Vol. 5, Issue. , p. 27.
    Tagliapietra, Valentina Rosà, Roberto Rossi, Chiara Rosso, Fausta Hauffe, Heidi Christine Tommasini, Michele Versini, Walter Cristallo, Attilio Fabio and Rizzoli, Annapaola 2018. Emerging Rodent-Borne Viral Zoonoses in Trento, Italy. EcoHealth,
    Lovrić, Z. Kolarić, B. Kosanović Ličina, M. L. Tomljenović, M. Đaković Rode, O. Danis, K. Kaić, B. and Tešić, V. 2018. An outbreak of haemorrhagic fever with renal syndrome linked with mountain recreational activities in Zagreb, Croatia, 2017. Epidemiology and Infection, Vol. 146, Issue. 10, p. 1236.
    Imholt, Christian Reil, Daniela Plašil, Pavel Rödiger, Kerstin and Jacob, Jens 2017. Long-term population patterns of rodents and associated damage in German forestry. Pest Management Science, Vol. 73, Issue. 2, p. 332.
    Reil, Daniela Rosenfeld, Ulrike M. Imholt, Christian Schmidt, Sabrina Ulrich, Rainer G. Eccard, Jana A. and Jacob, Jens 2017. Puumala hantavirus infections in bank vole populations: host and virus dynamics in Central Europe. BMC Ecology, Vol. 17, Issue. 1,
    REIL, D. IMHOLT, C. ROSENFELD, U. M. DREWES, S. FISCHER, S. HEUSER, E. PETRAITYTE-BURNEIKIENE, R. ULRICH, R. G. and JACOB, J. 2017. Validation of the Puumala virus rapid field test for bank voles in Germany. Epidemiology and Infection, Vol. 145, Issue. 03, p. 434.
    Monchatre-Leroy, E. Crespin, L. Boué, F. Marianneau, P. Calavas, D. and Hénaux, V. 2017. Spatial and Temporal Epidemiology of Nephropathia Epidemica Incidence and Hantavirus Seroprevalence in Rodent Hosts: Identification of the Main Environmental Factors in Europe. Transboundary and Emerging Diseases, Vol. 64, Issue. 4, p. 1210.
    Swart, Arno Bekker, Dick L. Maas, Miriam de Vries, Ankje Pijnacker, Roan Reusken, Chantal B. E. M. and van der Giessen, Joke W. B. 2017. Modelling human Puumala hantavirus infection in relation to bank vole abundance and masting intensity in the Netherlands. Infection Ecology & Epidemiology, Vol. 7, Issue. 1, p. 1287986.
    Onodera, Rokuya Akimoto, Yuka Shimada, Takuya and Saitoh, Takashi 2017. Different population responses of three sympatric rodent species to acorn masting—the role of tannin tolerance. Population Ecology, Vol. 59, Issue. 1, p. 29.
    Drewes, S. Turni, H. Rosenfeld, U. M. Obiegala, A. Straková, P. Imholt, C. Glatthaar, E. Dressel, K. Pfeffer, M. Jacob, J. Wagner-Wiening, C. and Ulrich, R. G. 2017. Reservoir-Driven Heterogeneous Distribution of Recorded Human Puumala virus Cases in South-West Germany. Zoonoses and Public Health, Vol. 64, Issue. 5, p. 381.
    Allen, Robert B. Millard, Peter and Richardson, Sarah J. 2017. Progress in Botany Vol. 79. Vol. 79, Issue. , p. 233.
    Drewes, Stephan Straková, Petra Drexler, Jan F. Jacob, Jens and Ulrich, Rainer G. 2017. In Loeffler’s Footsteps – Viral Genomics in the Era of High-Throughput Sequencing. Vol. 99, Issue. , p. 61.
    Reil, D. Imholt, C. Drewes, S. Ulrich, R. G. Eccard, J. A. and Jacob, J. 2016. Environmental conditions in favour of a hantavirus outbreak in 2015 in Germany?. Zoonoses and Public Health, Vol. 63, Issue. 2, p. 83.
    Bogdziewicz, Michał and Szymkowiak, Jakub 2016. Oak acorn crop and Google search volume predict Lyme disease risk in temperate Europe. Basic and Applied Ecology, Vol. 17, Issue. 4, p. 300.
    Voutilainen, Liina Kallio, Eva R. Niemimaa, Jukka Vapalahti, Olli and Henttonen, Heikki 2016. Temporal dynamics of Puumala hantavirus infection in cyclic populations of bank voles. Scientific Reports, Vol. 6, Issue. 1,
    Mgbemene, Chigbo A. Nnaji, Chidozie C. and Nwozor, Chekwubechukwu 2016. Industrialization and its Backlash: Focus on Climate Change and its Consequences. Journal of Environmental Science and Technology, Vol. 9, Issue. 4, p. 301.
    Bai, Yuntao Xu, Zhiguang Lu, Bo Sun, Qinghua Tang, Wenge Liu, Xiaobo Yang, Weizhong Xu, Xinyi Liu, Qiyong and Freiberg, Alexander N 2015. Effects of Climate and Rodent Factors on Hemorrhagic Fever with Renal Syndrome in Chongqing, China, 1997–2008. PLOS ONE, Vol. 10, Issue. 7, p. e0133218.
    Weber de Melo, Vanessa Sheikh Ali, Hanan Freise, Jona Kühnert, Denise Essbauer, Sandra Mertens, Marc Wanka, Konrad M. Drewes, Stephan Ulrich, Rainer G. and Heckel, Gerald 2015. Spatiotemporal dynamics of Puumala hantavirus associated with its rodent host,Myodes glareolus. Evolutionary Applications, Vol. 8, Issue. 6, p. 545.
    Tian, Huai-Yu Yu, Peng-Bo Luis, Angela D. Bi, Peng Cazelles, Bernard Laine, Marko Huang, Shan-Qian Ma, Chao-Feng Zhou, Sen Wei, Jing Li, Shen Lu, Xiao-Ling Qu, Jian-Hui Dong, Jian-Hua Tong, Shi-Lu Wang, Jing-Jun Grenfell, Bryan Xu, Bing and Scarpino, Samuel V. 2015. Changes in Rodent Abundance and Weather Conditions Potentially Drive Hemorrhagic Fever with Renal Syndrome Outbreaks in Xi’an, China, 2005–2012. PLOS Neglected Tropical Diseases, Vol. 9, Issue. 3, p. e0003530.
    Download full list
    ×
  • Get access
    Add to cart USD35.00
    Check if you have access via personal or institutional login
    Log in Register Recommend to librarian

Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate

  • K. TERSAGO (a1), R. VERHAGEN (a1), A. SERVAIS (a2), P. HEYMAN (a3), G. DUCOFFRE (a4) and H. LEIRS (a1) (a5)...
Summary

Recently, human cases of nephropathia epidemica (NE) due to Puumala virus infection in Europe have increased. Following the hypothesis that high reservoir host abundance induces higher transmission rates to humans, explanations for this altered epidemiology must be sought in factors that cause bank vole (Myodes glareolus) abundance peaks. In Western Europe, these abundance peaks are often related to high tree seed production, which is supposedly triggered by specific weather conditions. We evaluated the relationship between tree seed production, climate and NE incidence in Belgium and show that NE epidemics are indeed preceded by abundant tree seed production. Moreover, a direct link between climate and NE incidence is found. High summer and autumn temperatures, 2 years and 1 year respectively before NE occurrence, relate to high NE incidence. This enables early forecasting of NE outbreaks. Since future climate change scenarios predict higher temperatures in Europe, we should regard Puumala virus as an increasing health threat.

Copyright
COPYRIGHT: © 2008 Cambridge University Press
Corresponding author
*Author for correspondence: K. Tersago, University of Antwerp, Department of Biology, Evolutionary Ecology Group, Groenenborgerlaan 171, 2020 Antwerp, Belgium. (Email: Katrien.Tersago@ua.ac.be)
References
Hide All
1.Woolhouse, MEJ, Gowtage-Sequeria, S. Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 2005; 11: 1842–1847.
2.Vorou, RM, Papavassiliou, VG, Tsiodras, S. Emerging zoonoses and vector-borne infections affecting humans in Europe. Epidemiology and Infection 2007; 135: 1231–1247.
3.Mills, JN. Regulation of rodent-borne viruses in the natural host: implications for human disease. Archives of Virology (Suppl.) 2005; 19: 45–57.
4.Mailles, A, et al. Larger than usual increase in cases of Hantavirus infections in Belgium, France and Germany, June 2005. Eurosurveillance 2005; 10: 198–200.
5.Heyman, P, et al. Haemorrhagic fever with renal syndrome: an analysis of the outbreaks in Belgium, France, Germany, the Netherlands and Luxembourg in 2005. Eurosurveillance 2007; 12: 15–16.
6.Vapalahti, O, et al. Hantavirus infections in Europe. Lancet Infectious Diseases 2003; 3: 653–661.
7.Heyman, P, et al. Incidence of hantavirus infections in Belgium. Virus Research 2001; 77: 71–80.
8.Linard, C, et al. Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 2007; 6: 15.
9.Olsson, GE, et al. Human hantavirus infections, Sweden. Emerging Infectious Diseases 2003; 9: 1395–1401.
10.Linard, C, et al. Environmental conditions and Puumala virus transmission in Belgium. International Journal of Health Geographics 2007; 6: 55.
11.Davis, S, Calvet, E, Leirs, H. Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector Borne and Zoonotic Diseases 2005; 5: 305–314.
12.Escutenaire, S, et al. Spatial and temporal dynamics of Puumala hantavirus infection in red bank vole (Clethrionomys glareolus) populations in Belgium. Virus Research 2000; 67: 91–107.
13.Sauvage, F, Langlais, M, Pontier, D. Predicting the emergence of human hantavirus disease using a combination of viral dynamics and rodent demographic patterns. Epidemiology and Infection 2007; 135: 46–56.
14.Gavrilovskaya, IN, et al. Pathogenesis of hemorrhagic fever with renal syndrome virus infection and mode of horizontal transmission of hantavirus in bank voles. Archives of Virology (Suppl.) 1990; 1: 57–62.
15.Yoccoz, NG, et al. Effects of food addition on the seasonal density-dependent structure of bank vole Clethrionomys glareolus populations. Journal of Animal Ecology 2001; 70: 713–720.
16.Jensen, TS. Seed production and outbreaks of non-cyclic rodent populations in deciduous forests. Oecologia 1982; 52: 184–192.
17.Pucek, Z, et al. Rodent population dynamics in a primeval deciduous forest (Bialowieza national park) in relation to weather, seed crop and predation. Acta Theriologica 1993; 38: 199–232.
18.Verhagen, R, Leirs, H, Verheyen, W. Demography of Clethrionomys glareolus in Belgium. Polish Journal of Ecology 2000; 48: 113–123.
19.Crespin, L, et al. Survival in fluctuating bank vole populations: seasonal and yearly variations. Oikos 2002; 98: 467–479.
20.Prévot-Julliard, AC, et al. Delayed maturation in female bank voles: optimal decision or social constraint? Journal of Animal Ecology 1999; 68: 684–697.
21.Bujalska, G, Saitoh, T. Territoriality and its consequences. Polish Journal of Ecology 2000; 48: 37–49.
22.Clement, J, et al. Predicting hantavirus outbreaks and Lyme borreliosis peaks in Belgium – and Europe: of mast, mice and men. In: Abstracts of the 7th International Congress on Hantaviruses, Buenos Aires, Argentina, 13–15 June 2007, Abstract S1-O2, p. 21.
23.Johnson, PS, Shifley, SR, Rogers, R. The Ecology of Silviculture of Oaks. New York: CABI Publishers, 2002, pp. 61–64.
24.Koenig, WD, Knops, JMH. The mystery of masting in trees. American Scientist 2005; 93: 340–347.
25.Piovesan, G, Adams, JM. Masting behaviour in beech: linking reproduction and climatic variation. Botany 2001; 79: 1039–1047.
26.Övergaard, R, Gemmel, P, Karlsson, M. Effects of weather conditions on mast year frequency in beech (Fagus sylvatica L.) in Sweden. Forestry 2007; 80: 555–565.
27.Kallio, ER, et al. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. Journal of General Virology 2006; 87: 2127–2134.
28.SAS Institute. SAS/STAT User's guide, version 9.1. SAS Institute Inc., Cary, 2003.
29.Agresti, A. Categorical Data Analysis, 2nd edn, New Jersey: John Wiley & Sons, 2002, pp. 324–325.
30.Clotfelter, ED, et al. Acorn mast drives long-term dynamics of rodent and songbird populations. Oecologia 2007; 154: 493–503.
31.Tamerius, JD, et al. Climate and human health: synthesizing environmental complexity and uncertainty. Stochastic Environmental research and Risk Assessment 2007; 21: 601–613.
32.Engelthaler, DM, et al. Climatic and environmental patterns associated with hantavirus pulmonary syndrome, Four Corners region, United States. Emerging Infectious Diseases 1999; 5: 87–94.
33.Hjelle, B, Glass, GE. Outbreak of hantavirus infection in the four corners region of the United States in the wake of the 1997–1998 El Nino-southern oscillation. Journal of Infectious Diseases 2000; 181: 1569–1573.
34.Yates, TL, et al. The ecology and evolutionary history of an emergent disease: Hantavirus pulmonary syndrome. BioScience 2002; 52: 989–998.
35.Glass, GE, et al. Persistently highest risk areas for hantavirus pulmonary syndrome: Potential sites for refugia. Ecological Applications 2007; 17: 129–139.
36.Zaitchik, BF, et al. Europe's 2003 heat wave: a satellite view of impacts and land-atmosphere feedbacks. International Journal of Climatology 2006; 26: 743–769.
37.Reichstein, M, et al. Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Global Change Biology 2007; 13: 634–651.
38.Abu Sin, M, et al. Risk factors for hantavirus infection in Germany, 2005. Emerging Infectious Diseases 2007; 13: 1364–1366.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Epidemiology & Infection
  • ISSN: 0950-2688
  • EISSN: 1469-4409
  • URL: /core/journals/epidemiology-and-infection
Please enter your name
Please enter a valid email address
Who would you like to send this to? *

CAPTCHA *

Skip to the audio challenge
×

Keywords

Metrics

Altmetric attention score

Cancel
Confirm
×