Environmental effects on parasitic disease transmission exemplified by schistosomiasis in western China

Environmental effects on the transmission of many parasitic diseases are well recognized, but the role of specific factors like climate and agricultural practices in modulating transmission is seldom characterized quantitatively. Based on studies of Schistosoma japonicum transmission in irrigated agricultural environments in western China, a mathematical model was used to quantify environmental impacts on transmission intensity. The model was calibrated by using field data from intervention studies in three villages and simulated to predict the effects of alternative control options. Both the results of these interventions and earlier epidemiological findings confirm the central role of environmental factors, particularly those relating to snail habitat and agricultural and sanitation practices. Moreover, the findings indicate the inadequacy of current niclosamide-praziquantel strategies alone to achieve sustainable interruption of transmission in some endemic areas. More generally, the analysis suggests a village-specific index of transmission potential and how this potential is modulated by time-varying factors, including climatological variables, seasonal water-contact patterns, and irrigation practices. These time-variable factors, a village's internal potential, and its connectedness to its neighbors provide a framework for evaluating the likelihood of sustained schistosomiasis transmission and suggest an approach to quantifying the role of environmental factors for other parasitic diseases.

[1]  Z. Andrade The situation of hepatosplenic schistosomiasis in Brazil today. , 1998, Memorias do Instituto Oswaldo Cruz.

[2]  R M May,et al.  Helminth infections of humans: mathematical models, population dynamics, and control. , 1985, Advances in parasitology.

[3]  S. Liang,et al.  Re-emerging schistosomiasis in hilly and mountainous areas of Sichuan, China. , 2006, Bulletin of the World Health Organization.

[4]  C. King,et al.  Factors affecting infection or reinfection with Schistosoma haematobium in coastal Kenya: survival analysis during a nine-year, school-based treatment program. , 2006, The American journal of tropical medicine and hygiene.

[5]  P. Hosseini,et al.  Seasonality and the dynamics of infectious diseases. , 2006, Ecology letters.

[6]  F. Zheng,et al.  Schistosomiasis control in China. , 1999, Parasitology international.

[7]  R. Snow,et al.  Infant parasite rates and immunoglobulin M seroprevalence as a measure of exposure to Plasmodium falciparum during a randomized controlled trial of insecticide-treated bed nets on the Kenyan coast. , 1996, The American journal of tropical medicine and hygiene.

[8]  N. Nicholls,et al.  Weather Variability, Tides, and Barmah Forest Virus Disease in the Gladstone Region, Australia , 2005, Environmental health perspectives.

[9]  S. Liang,et al.  Estimating the distribution of worm burden and egg excretion of Schistosoma japonicum by risk group in Sichuan Province, China , 2002, Parasitology.

[10]  Ilkka Hanski,et al.  Spatially realistic theory of metapopulation ecology , 2001, Naturwissenschaften.

[11]  A. Barbour Modeling the transmission of schistosomiasis: an introductory view. , 1996, The American journal of tropical medicine and hygiene.

[12]  D. Gurarie,et al.  Heterogeneous model of schistosomiasis transmission and long-term control: the combined influence of spatial variation and age-dependent factors on optimal allocation of drug therapy , 2004, Parasitology.

[13]  F. Richards,et al.  Control of onchocerciasis today: status and challenges. , 2001, Trends in parasitology.

[14]  J. Patz,et al.  Effects of environmental change on emerging parasitic diseases. , 2000, International journal for parasitology.

[15]  Dirk Engels,et al.  Morbidity control of schistosomiasis in China. , 2002, Acta tropica.

[16]  R. May Togetherness among Schistosomes: its effects on the dynamics of the infection , 1977 .

[17]  M. Woolhouse,et al.  Population dynamics model for Bulinus globosus, intermediate host for Schistosoma haematobium, in river habitats. , 1990, Acta tropica.

[18]  Fabio Zicker,et al.  Strategic emphases for tropical diseases research: a TDR perspective. , 2002, Trends in parasitology.

[19]  H. Tanaka,et al.  From discovery to eradication of schistosomiasis in Japan: 1847-1996. , 1997, International journal for parasitology.

[20]  M E Woolhouse Mathematical models of transmission dynamics and control of schistosomiasis. , 1996, The American journal of tropical medicine and hygiene.

[21]  R. May,et al.  Infectious Diseases of Humans: Dynamics and Control , 1991, Annals of Internal Medicine.

[22]  B. Goodger,et al.  The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  Edmund Seto,et al.  Disease transmission models for public health decision making: toward an approach for designing intervention strategies for Schistosomiasis japonica. , 2002, Environmental health perspectives.

[24]  Zheng Feng,et al.  Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People's Republic of China. , 2002, Acta tropica.

[25]  M. Woolhouse,et al.  On estimating the basic reproduction number for Schistosoma haematobium , 1996, Tropical medicine & international health : TM & IH.

[26]  R. Spear,et al.  Transport of Schistosoma japonicum cercariae and the feasibility of niclosamide for cercariae control. , 2005, Parasitology international.

[27]  You-sheng Liang,et al.  Susceptibility of Schistosoma japonicum to praziquantel in China , 2001, Tropical medicine & international health : TM & IH.

[28]  M. Gilpin,et al.  Metapopulation Biology: Ecology, Genetics, and Evolution , 1997 .

[29]  M. Todd,et al.  Drugs for the control of parasitic diseases: current status and development in schistosomiasis. , 2003, Trends in parasitology.

[30]  D. Molyneux “Neglected” diseases but unrecognised successes—challenges and opportunities for infectious disease control , 2004, The Lancet.

[31]  A. Fenwick New initiatives against Africa's worms. , 2006, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[32]  M. van Boven,et al.  Avian influenza A virus (H7N7) epidemic in The Netherlands in 2003: course of the epidemic and effectiveness of control measures. , 2004, The Journal of infectious diseases.

[33]  Song Liang,et al.  A quantitative framework for a multi-group model of Schistosomiasis japonicum transmission dynamics and control in Sichuan, China. , 2002, Acta tropica.

[34]  W. Martens Health and Climate Change: Modelling the Impacts of Global Warming and Ozone Depletion , 1998 .

[35]  G Macdonald,et al.  The dynamics of helminth infections, with special reference to schistosomes. , 1965, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[36]  Roger L. H. Dennis,et al.  Probability of site occupancy in the large heath butterfly Coenonympha tullia determined from geographical and ecological data , 1999 .

[37]  Andrew P. Morse,et al.  A weather-driven model of malaria transmission , 2004, Malaria Journal.

[38]  R. Snow,et al.  A climate-based distribution model of malaria transmission in sub-Saharan Africa. , 1999, Parasitology today.

[39]  Laurie Geller,et al.  Under the Weather: Climate, Ecosystems, and Infectious Disease , 2001 .

[40]  D. Earn,et al.  A simple model for complex dynamical transitions in epidemics. , 2000, Science.

[41]  S. Liang,et al.  A Spatial-Temporal Model for Assessing the Effects of Intervillage Connectivity in Schistosomiasis Transmission , 2006 .

[42]  A. Fulford,et al.  The development of an age structured model for schistosomiasis transmission dynamics and control and its validation for Schistosoma mansoni , 1995, Epidemiology and Infection.

[43]  S. Liang,et al.  Factors influencing the transmission of Schistosoma japonicum in the mountains of Sichuan Province of China. , 2004, The American journal of tropical medicine and hygiene.

[44]  A. Hubbard,et al.  Genetic and household risk factors for Schistosoma japonicum infection in the presence of larger scale environmental differences in the mountainous transmission areas of China. , 2005, The American journal of tropical medicine and hygiene.

[45]  W. Reisen,et al.  Relationships among weather, mosquito abundance, and encephalitis virus activity in California: Kern County 1990-98. , 2000, Journal of the American Mosquito Control Association.

[46]  Edmund Seto,et al.  A multi‐group model of Schistosoma japonicum transmission dynamics and control: model calibration and control prediction , 2005, Tropical medicine & international health : TM & IH.

[47]  B. Grenfell,et al.  Re-assessing the global prevalence and distribution of lymphatic filariasis , 1996, Parasitology.