Field transmission intensity of Schistosoma japonicum measured by basic reproduction ratio from modified Barbour’s model

Particle and Fibre Toxicology

Xiao-Nong Zhou²  Guo-Jing Yang¹  Yu-Jiang Liu³  Yu-Ying He³  Shu-Jing Gao³ 

[1] Jiangsu Institute of Parasitic Diseases, Key Laboratory on Control Technology for Parasitic Diseases, Ministry of Health, Wuxi, Jiangsu 214064, China;Key Laboratory of Parasite and Vector Biology, MOH; WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, China;Key Laboratory of Jiangxi Province for Numerical Simulation and Emulation Techniques, Gannan Normal University, Ganzhou 341000, China

关键词: People’s Republic of China;    Schistosomiasis elimination;    Parameter estimation;    Basic reproduction ratio;    Prevalence;    Mathematical model;    Schistosoma japonicum;   

Others  :  1227959
DOI  :  10.1186/1756-3305-6-141

 received in 2013-01-10, accepted in 2013-05-04,  发布年份 2013

【 摘 要 】

Background

Schistosomiasis japonica, caused by infection with Schistosoma japonicum, is still recognized as a major public health problem in the Peoples’ Republic of China. Mathematical modelling of schistosomiasis transmission has been undertaken in order to assess and project the effects of various control strategies for elimination of the disease. Seasonal fluctuations in transmission may have the potential to impact on the population dynamics of schistosomiasis, yet no model of S. japonicum has considered such effects. In this paper, we characterize the transmission dynamics of S. japonicum using a modified version of Barbour’s model to account for seasonal variation (SV), and investigate the effectiveness of the control strategy adopted in Liaonan village of Xingzi county, Jiangxi Province.

Methods

We use mathematical tools for stability analysis of periodic systems and derive expressions for the basic reproduction ratio of S. japonicum in humans; we parameterise such expressions with surveillance data to investigate the conditions for persistence or elimination of the disease in the study village. We perform numerical simulations and parametric sensitivity analysis to understand local transmission conditions and compare values of the basic reproductive ratio with and without seasonal fluctuations.

Results

The explicit formula of the basic reproduction ratio for the SV-modified Barbour’s model is derived. Results show that the value of the basic reproduction ratio, R₀, of Liaonan village, Xingzi county is located between 1.064 and 1.066 (very close to 1), for schistosomiasis transmission during 2006 to 2010, after intensification of control efforts.

Conclusions

Our modified version of the Barbour model to account for seasonal fluctuations in transmission has the potential to provide better estimations of infection risk than previous models. Ignoring seasonality tends to underestimate R₀ values albeit only marginally. In the absence of simultaneous R₀ estimations for villages not under control interventions (such villages do not currently exist in China), it is difficult to assess whether control strategies have had a substantial impact on levels of transmission, as the parasite population would still be able to maintain itself at an endemic level, highlighting the difficulties faced by elimination efforts.

【 授权许可】

   
2013 Gao et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium: The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009, 460:345-351.
• [2]Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J: The public health significance and control of schistosomiasis in China– then and now. Acta Trop 2005, 96:97-105.
• [3]Zhou XN, Guo JG, Wu XH, Jiang QW, Zheng J, Dang H, Wang XH, Xu J, Zhu HQ, Wu GL, Li YS, Xu XJ, Chen HG, Wang TP, Zhu YC, Qiu DC, Dong XQ, Zhao GM, Zhang SJ, Zhao NQ, Xia G, Wang LY, Zhang SQ, Lin DD, Chen MG, Hao Y: Epidemiology of schistosomiasis in the People’s Republic of China, 2004. Emerg Infect Dis 2007, 13:1470-1476.
• [4]Wang TP, Cao ZG, Chen HG, Zhou XN: Changes of control strategy and improvement of schistosomiasis control in China. Chin J Schisto Contrl 2009, 21:241-242.
• [5]Li SZ, Luz A, Wang XH, Xu LL, Wang Q, Qian YJ, Wu XH, Guo JG, Xia G, Wang LY, Zhou XN: Schistosomiasis in China: acute infections during 2005–2008. Chin Med J (Engl) 2009, 122:1009-1014.
• [6]Zhang ZJ, Clark AB, Bivand R, Chen Y, Carpenter TE, Peng WX, Zhou YB, Zhao GM, Jiang QW: Nonparametric spatial analysis to detect high-risk regions for schistosomiasis in Guichi, China. Trans R Soc Trop Med Hyg 2009, 103:1045-1052.
• [7]He YX, Salafsky B, Ramaswamy K: Host-parasite relationships of Schistosoma japonicum in mammalian hosts. Trends Parasitol 2001, 17:320-324.
• [8]Xiao DL, Yu Q, Dang H, Guo JG, Zhou XN, Wang LY: Schistosomiasis situation in People’s Republic of China in 2003 [in Chinese]. Chin J Schisto Contrl. 2004, 16:401-405.
• [9]Wang LD, Chen HG, Guo JG, Zeng XJ, Hong XL, Xiong JJ, Wu XH, Wang XH, Wang LY, Xia G, Hao Y, Chin DP, Zhou XN: A strategy to control transmission of Schistosoma japonicum in China. N Engl J Med 2009, 360:121-128.
• [10]Gray DJ, Williams GM, Li Y, McManus DP: Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. PLoS ONE 2008, 3:e4058.
• [11]Liang S, Maszle D, Spear RC: A quantitative framework for a multi-group model of Schistosomiasis japonica transmission dynamics and control in Sichuan, China. Acta Trop 2002, 82:263-277.
• [12]Liang S, Spear RC, Seto E, Hubbard A, Qiu D: A multi-group model of Schistosoma japonicum transmission dynamics and control: model calibration and control prediction. Trop Med Int Health 2005, 10:263-278.
• [13]Spear RC, Hubbard A, Liang S, Seto E: Disease transmission models for public health decision making: toward an approach for designing intervention strategies for schistosomiasis japonica. Environ Health Perspect 2002, 110:907-915.
• [14]Williams GM, Sleigh AC, Li YS, Feng Z, Davis GM, Chen H, Ross AGP, Bergquist R, McManus DP: Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People’s Republic of China. Acta Trop 2002, 82:253-262.
• [15]Feng Z, Li CC, Milner FA: Schistosomiasis models with two migrating human groups. Math Comput Model 2005, 41:1213-1230.
• [16]Chiyaka ET, Garira W: Mathematical analysis of the transmission dynamics of schistosomiasis in the human-snail hosts. J Biol Syst 2009, 17:397-423.
• [17]Dublin LI, Lotka AJ: On the true rate of natural increase. J Am Stat Assoc New Series 1925, 150:305-339.
• [18]Ross R: The prevention of malaria. London: John Murray; 1911.
• [19]Sharp FR, Lotka AJ: A problem in age distribution. Phil Mag 1911, 6:435-438.
• [20]Heesterbeek JAP, Roberts MG: Threshold quantities for helminth infections. J Math Biol 1995, 33:415-434.
• [21]MacDonald G: The analysis of equilibrium in malaria. Trop Dis Bull 1952, 49:813-829.
• [22]Wang JY, WD : The effect of population dispersal on the spread of a disease. J Math Anal Appl 2005, 308:343-364.
• [23]Mukandavire Z, Chiyaka C, Garira W, Musuka G: Mathematical analysis of a sex-structured HIV/AIDS model with a discrete time delay. Nonlinear Anal-Theor 2009, 71:1082-1093.
• [24]Gao SJ, Liu YJ, Nieto JJ, Andrade H: Seasonality and mixed vaccination strategy in an epidemic model with vertical transmission. Math Comput Simulat 2011, 81:1855-1868.
• [25]Bacaër N, Dads EHA: On the biological interpretation of a definition for the parameterR0in periodic population models. J Math Biol 2012, 65:601-621.
• [26]Heesterbeek JAP: A brief history ofR0and a recipe for its calculation. Acta Biotheor 2002, 50:189-204.
• [27]Inaba H: On a new perspective of the basic reproduction number in heterogeneous environments. J Math Biol 2012, 65:309-348.
• [28]Anderson RM, May RM: Infectious Disease of Humans: Dynamics and Control. Oxford: Oxford University Press; 1991.
• [29]Diekmann O, Heesterbeek JAP, Metz JAJ: On the definition and the computation of the basic reproduction ratioR0in models for infectious diseases in heterogeneous populations. J Math Biol 1990, 28:365-382.
• [30]MacDonald G: The dynamics of helminth infections, with special reference to schistosomes. Trans R Soc Trop Med Hyg 1965, 59:489-506.
• [31]Nåsell I: On eradication of schistosomiasis. Theor Popul Biol 1976, 10:133-144.
• [32]Cohen JE: Mathematical models of schistosomiasis. Annu Rev Ecol Syst 1977, 8:209-233.
• [33]May RM: Togetherness among the schistosomes: its effects on the dynamics of the infection. Math Biosci 1977, 35:301-343.
• [34]Barbour AD: Macdonald's model and the transmission of bilharzia. Trans R Soc Trop Med Hyg 1978, 72:6-15.
• [35]Anderson RM, May RM: Helminth infections of humans: mathematical models, population dynamics, and control. Adv Parasitol 1985, 24:1-101.
• [36]Chan MS, Guyatt HL, Bundy DAP, Booth M, Fulford AJC, Medley GF: The development of an age structured model for schistosomiasis transmission dynamics and control and its validation for Schistosoma mansoni. Epidemiol Infect 1995, 115:325-344.
• [37]Chan MS, Montresor A, Savioli L, Bundy DAP: Planning chemotherapy-based schistosomiasis control: validation of a mathematical model using data on Schistosoma haematobium from Pemba, Tanzania. Epidemiol Infect 1999, 123:487-497.
• [38]French MD, Churcher TS, Gambhir M, Fenwick A, Webster JP, Kabatereine NB, Basáñez MG: Observed reductions in Schistosoma mansoni transmission from large-scale administration of praziquantel in Uganda: A mathematical modelling study. PLoS Negl Trop Dis 2010, 4:e897.
• [39]Woolhouse MEJ: On the application of mathematical models of schistosome transmission dynamics. I. Natural transmission. Acta Trop 1991, 49:241-270.
• [40]Woolhouse MEJ: On the application of mathematical models of schistosome transmission dynamics. II. Control. Acta Trop 1992, 50:189-204.
• [41]Barbour AD: Modelling the transmission of schistosomiasis: an introductory view. Am J Trop Med Hyg 1996, 55(5 Suppl):135-143.
• [42]Riley S, Carabin H, Marshall C, Olveda R, Willingham AL, McGarvey ST: Estimating and modeling the dynamics of the intensity of infection with Schistosoma japonicum in villagers of Leyte, Philippines. Part II: Intensity-specific transmission of S. japonicum. The schistosomiasis transmission and ecology project. Am J Trop Med Hyg 2005, 72:754-761.
• [43]Riley S, Carabin H, Belisle P, Joseph L, Tallo V, Balolong E, Willingham AL, Fernandez TJ, Gonzales RO, Olveda R, McGarvey ST: Multi-host transmission dynamics of Schistosoma japonicum in Samar province, the Philippines. PLoS Med 2008, 5:e18.
• [44]Ishikawa H, Ohmae H, Pangilinan R, Redulla A, Matsuda H: Modeling the dynamics and control of Schistosoma japonicum transmission on Bohol island, the Philippines. Parasitol Int 2006, 55:23-29.
• [45]Wang LD, Utzinger J, Zhou XN: Schistosomiasis control: experiences and lessons from China. Lancet 2008, 372:1793-1795.
• [46]Wang TP, Vang Johansen M, Zhang SQ, Wang FF, Wu WD, Zhang GH, Pan XP, Ju Y, Ornbjerg N: Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui province, China. Acta Trop 2005, 96:198-204.
• [47]Wang XH, Wu XH, Zhou XN: Bayesian estimation of community prevalences of Schistosoma japonicum infection in China. Int J Parasitol 2006, 36:895-902.
• [48]Vandemark LM, Jia TW, Zhou XN: Social science implications for control of helminth infections in Southeast Asia. Adv Parasitol 2010, 73:137-70.
• [49]Zhou XN, Malone JB, Kristensen TK, Bergquist NR: Application of geographic information systems and remote sensing to schistosomiasis control in China. Acta Trop 2001, 79:97-106.
• [50]Wang WD, Zhao XQ: Threshold dynamics for compartmental epidemic models in periodic environments. J Dyn Diff Equat 2008, 20:699-717.
• [51]Tao B, Jiang QL, Luo CJ, Yin ZH, Wang JM: Endemic situation of schistosomiasis in Xingzi Country. Chin J Schisto Contrl 2009, 21:62-63.
• [52]Katz N, Chaves A, Pellegrino J: A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 1972, 14:397-400.
• [53]Lin DD, Liu YM, Hu F, Li YF, Tao B, Yuan M, Xie SY, Huang MJ, Jiang QL, Li JY, Gao ZL, Wang JM: Evaluation on application of common diagnosis methods for schistosomiasis japonica in endemic areas of China. III. Analysis and evaluation of underestimation of prevalence of Schistosoma japonicum infection by routine Kato-Katz technique. Chin J Parasitol Parasitic Dis 2011, 23:642-647.
• [54]Ministry of Health, C: Manual of Schistosomiais Control and Prevention, in: Control, B.o.D. (Ed.). 3rd edition. Shanghai: Shanghai Scientific and Technical Publishers; 2000:72-76.
• [55]Xu J, Li SZ, Huang YX, Cao ZG, Tu ZW, Wu CG, Miu F, Dang H, Zhang LJ, Chen Z, Wang LY, Guo JG, Zhou XN: Risk evaluation of schistosomiasis japonica in potential endemic areas in China. Chin J Parasitol Parasitic Dis 2012, 30:428–33-437.
• [56]Ministry of Health: National guideline for snail survey, control, population infection screen and chemotherapy of schistosomiasis (Trial), in: Control, B.o.D. (Ed.). Beijing: Ministry of Health; 2005.
• [57]Wu KC: Mathematical model and transmission dynamics of schistosomiasis and its application. Chin Trop Med 2005, 5:837-844.
• [58]Seto EYW, Remais JV, Carlton EJ, Wang S, Liang S, Brindley PJ, Qiu DC, Spear RC, Wang LD, Wang TP, Chen HG, Dong XQ, Wang LY, Hao Y, Bergquist R, Zhou XN: Toward sustainable and comprehensive control of schistosomiasis in China: lessons from Sichuan. PLoS Negl Trop Dis 2011, 5:e1372.
• [59]Wang LD, Guo JG, Wu XH, Chen HG, Wang TP, Zhu SP, Zhang ZH, Steinmann P, Yang GJ, Wang SP, Wu ZD, Wang LY, Hao Y, Bergquist R, Utzinger J, Zhou XN: China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop Med Int Health 2009, 14:1475-1483.
• [60]Feng Z, Li CC, Milner FA: Effects of density and age dependence on the transmission dynamics of schistosomes. Math Biosci 2002, 177–178:271-286.
• [61]Van den Driessche P, Watmough J: Reproduction numbers and sub-threshold endemic equilibiria for compartmental models of disease transmission. Math Biol 2002, 180:29-48.
• [62]Dye C: Vectorial capacity: must we measure all its components? Parasitol Today 1986, 2:203-209.
• [63]Woolhouse MEJ, Hasibeder G, Chandiwana SK: On estimating the basic reproduction number for Schistosoma haematobium. Trop Med Int Health 1996, 1:456-463.
• [64]Nåsell I: On the quasi-stationary distribution of the Ross malaria model. Math Biosci 1991, 107:187-207.
• [65]Nåsell I: On the quasi-stationary distribution of the stochastic logistic epidemic. Math Biosci 1999, 156:21-40.
• [66]Jacquez JA, Simon CP: The stochastic SI model with recruitment and deaths. I. Comparison with the closed SIS model. Math Biosci 1993, 117:77-125.
• [67]Ray KJ, Porco TC, Hong KC, Lee DC, Alemayehu W, Melese M, Lakew T, Yi E, House J, Chidambaram JD, Whitcher JP, Gaynor BD, Lietman TM: A rationale for continuing mass antibiotic distributions for trachoma. BMC Infect Dis 2007, 7:91. BioMed Central Full Text
• [68]Gambhir M, Michael E: Complex ecological dynamics and eradicability of the vector borne macroparasitic disease, lymphatic filariasis. PLoS ONE 2008, 3:e2874.
• [69]Zhou XN, Bergquist R, Tanner M: Elimination of tropical diseases through surveillance and response. Inf Dis Poverty 2013, 2:1. BioMed Central Full Text
• [70]Woolhouse ME, Hagan P: Seeking the ghost of worms past. Nat Med 1999, 5:1225-1227.
• [71]Mutapi F, Ndhlovu PD, Hagan P, Spicer JT, Mduluza T, Turner CM, Chandiwana SK, Woolhouse ME: Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J Infect Dis 1998, 178:289-293.
• [72]Zhou XN: Prioritizing research for “One health-One world”. Inf Dis Poverty 2012, 1:1. BioMed Central Full Text
• [73]Gray DJ, Williams GM, Li YS, Chen HG, Forsyth SJ, Li RS, Barnett AG, Guo JG, Ross AG, Feng Z, McManus DP: A cluster-randomised intervention trail against Schistosoma japonicum in the People's Republic of China: bovine and human transmission. PLoS ONE 2009, 4:e5900.
• [74]Jin YM, Lu K, Zhou WF, Fu ZQ, Liu JM, Shi YJ, Li H, Lin JJ: Comparison of recombinant proteins from Schistosoma japonicum for schistosomiasis diagnosis. Clin Vaccine Immunol 2010, 17:476-480.
• [75]McManus DP, Gray DJ, Ross AG, Williams GM, He HB, Li YS: Schistosomiasis research in the Dongting lake region and its impact on local and national treatment and control in China. PLoS Negl Trop Dis 2011, 5:e1053.
• [76]Rudge JW, Lu DB, Fang GR, Wang TP, Basáñez MG, Webster JP: Parasite genetic differentiation by host species and habitat type: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anhui Province, China. Mol Ecol 2009, 18:2134-2147.
• [77]Lu DB, Wang TP, Rudge JW, Donnelly CA, Fang GR, Webster JP: Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China–a two-year longitudinal parasitological survey. Parasitology 2010, 137:99-110.
• [78]APOC: Conceptual and operational framework of onchocerciasis elimination with ivermectin treatment. African Programme for Onchocerciasis Control (WHO/APOC). 2010. Available: http://www.who.int/apoc/oncho_elimination_report_english.pdf webcite (accessed 31 March 2013)
• [79]Butler CD: Infectious disease emergence and global change: thinking systemically in a shrinking world. Inf Dis Poverty 2012, 1:5. BioMed Central Full Text
• [80]Lara-Ramírez EE, Rodríguez-Pérez MA, Pérez-Rodríguez MA, Adeleke MA, Orozco-Algarra ME, Arrendondo-Jiménez JI, Guo X: Time series analysis of onchocerciasis data from Mexico: a trend towards elimination. PLoS Negl Trop Dis 2013, 7:e2033.
• [81]Gurarie D, Seto EY: Connectivity sustains disease transmission in environments with low potential for endemicity: modelling schistosomiasis with hydrologic and social connectivities. J R Soc Interface 2009, 6:495-508.