Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-05T08:35:35.511Z Has data issue: false hasContentIssue false
  • English
  • Français

A global sensitivity analysis for African sleeping sickness

Published online by Cambridge University Press:  16 November 2010

STEPHEN DAVIS ,
SERAP AKSOY  and
ALISON GALVANI
STEPHEN DAVIS*
Affiliation:
Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT 06520USA School of Mathematics and Geospatial Sciences, RMIT University, GPO Box 2476 V, Melbourne, Victoria 3001, Australia
SERAP AKSOY
Affiliation:
Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT 06520USA
ALISON GALVANI
Affiliation:
Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT 06520USA
*
*Corresponding author: School of Mathematical and Geospatial Sciences, Building 8, Level 9, Room 67, RMIT University, GPO Box 2476V, Melbourne, Victoria 3000, Australia. Tel: +61 (0)3 9925 2278. Fax: +61 (0)3 9925 2454. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

African sleeping sickness is a parasitic disease transmitted through the bites of tsetse flies of the genus Glossina. We constructed mechanistic models for the basic reproduction number, R0, of Trypanosoma brucei gambiense and Trypanosoma brucei rhodesiense, respectively the causative agents of West and East African human sleeping sickness. We present global sensitivity analyses of these models that rank the importance of the biological parameters that may explain variation in R0, using parameter ranges based on literature, field data and expertize out of Uganda. For West African sleeping sickness, our results indicate that the proportion of bloodmeals taken from humans by Glossina fuscipes fuscipes is the most important factor, suggesting that differences in the exposure of humans to tsetse are fundamental to the distribution of T. b. gambiense. The second ranked parameter for T. b. gambiense and the highest ranked for T. b. rhodesiense was the proportion of Glossina refractory to infection. This finding underlines the possible implications of recent work showing that nutritionally stressed tsetse are more susceptible to trypanosome infection, and provides broad support for control strategies in development that are aimed at increasing refractoriness in tsetse flies. We note though that for T. b. rhodesiense the population parameters for tsetse – species composition, survival and abundance – were ranked almost as highly as the proportion refractory, and that the model assumed regular treatment of livestock with trypanocides as an established practice in the areas of Uganda experiencing East African sleeping sickness.

Keywords

trypanosomiasisnext-generation matrixmathematical modelTrypanosoma brucei gambienseTrypanosoma brucei rhodesiense
Type
Research Article
Information
Parasitology , Volume 138 , Issue 4 , April 2011 , pp. 516 - 526
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akoda, K., Van den Bossche, P., Lyaruu, E. A., De Deken, R., Marcotty, T., Coosemans, M. and Van den Abbeele, J. (2009 a). Maturation of a Trypanosoma brucei infection to the infectious metacyclic stage is enhanced in nutritionally stressed tsetse flies. Journal of Medical Entomology 46, 1446–1449.CrossRefGoogle Scholar
Akoda, K., Van den Abbeele, J., Marcotty, T., De Deken, R., Sidibe, I. and Van den Bossche, P. (2009 b). Nutritional stress of adult female tsetse flies (Diptera: Glossinidae) affects the susceptibility of their offspring to trypanosomal infections. Acta Tropica 111, 263–267.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Clausen, P.-H., Adeyemi, I., Bauer, B., Breloeer, M., Salchow, F. and Staak, C. (1998). Host preferences of tsetse (Diptera: Glossinidae) based on bloodmeal identifications. Medical and Veterinary Entomology 12, 169–180.CrossRefGoogle ScholarPubMed
Cecchi, G., Paone, M., Franco, J. R., Fèvre, E. M., Diarra, A., Ruiz, J. A., Mattioli, R. C. and Simarro, P. P. (2009). Towards the Atlas of human African trypanosomiasis. International Journal of Health Geographics 8, 15. doi: 10.1186/1476-072X-8-15.CrossRefGoogle ScholarPubMed
Checchi, F., Filipe, J. A. N., Haydon, D. T., Chandramohan, D. and Chappuis, F. (2008). Estimates of the duration of the early and late stages of gambiense sleeping sickness. BMC Infectious Diseases 8, 16. doi: 10.1186/1471-2334-8-16.CrossRefGoogle ScholarPubMed
Dale, C., Welburn, S. C., Maudlin, I. and Milligan, P. J. M. (1995). The kinetics of maturation of trypanosome infections in tsetse. Parasitology 111, 187–191.CrossRefGoogle ScholarPubMed
Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical epidemiology of infectious diseases: model building, analysis and interpretation. John Wiley & Sons Ltd, New York, USA.Google Scholar
Diekmann, O., Heesterbeek, J. A. P. and Metz, J. A. J. (1990). On the definition and computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365–382.CrossRefGoogle ScholarPubMed
Durvasula, R. V., Gumbs, A., Panackal, A., Kruglov, O., Aksoy, S., Merrifield, R. B., Richards, F. F. and Beard, C. B. (1997). Prevention of insect-borne disease: an approach using transgenic symbiotic bacteria. Proceedings of the National Academy of Sciences, USA 94, 3274–3278.CrossRefGoogle ScholarPubMed
Fèvre, E. M., Picozzi, K., Jannin, J., Welburn, S. C. and Maudlin, I. (2006 a). Human African trypanosomiasis: epidemiology and control. Advances in Parasitology 61, 167–221.CrossRefGoogle ScholarPubMed
Fèvre, E. M., Tilley, A., Picozzi, K., Fyfe, J., Anderson, I., Magona, J. W., Shaw, D. J., Eisler, M. C. and Welburn, S. C. (2006 b). Central point sampling from cattle in livestock markets in areas of human sleeping sickness. Acta Tropica 9, 229–232.CrossRefGoogle Scholar
Fèvre, E. M., Odiit, M., Coleman, P. G., Woolhouse, M. E. J. and Welburn, S. C. (2008) Estimating the burden of rhodesiense sleeping sickness during an outbreak in Serere, eastern Uganda. BMC Public Health 8, 96. doi: 10.1186/1471-2458-8-96.CrossRefGoogle ScholarPubMed
Gubbins, S., Carpenter, S., Bayliss, M., Wood, J. L. and Mellor, P. S. (2008). Assessing the risk of bluetongue to UK livestock: uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. Interface 5, 363–371.Google Scholar
Hartemink, N. A., Randolph, S. E., Davis, S. and Heesterbeek, J. A. P. (2008). The basic reproduction number for complex disease systems: defining R0 for tick-borne infections. American Naturalist 171, 743–754.CrossRefGoogle ScholarPubMed
Kubi, C., Van den Abbeele, J., De Deken, R., Marcotty, T., Dorny, P. and Van den Bossche, P. (2009). The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection. Journal of Medical Entomology 46, 1446–1449.Google Scholar
Matser, A., Hartemink, N., Heesterbeek, J. A. P., Galvani, A. and Davis, S. (2009). Elasticity analysis in epidemiology: an application to tick-borne infections. Ecology Letters 12, 1–8.CrossRefGoogle ScholarPubMed
Okoth, J. O. and Kapaata, R. (1986). Trypanosome infection-rates in Glossina fuscipes fuscipes (Newst) in the Busoga sleeping sickness focus, Uganda. Annals of Tropical Medicine and Parasitology 80, 459–461.CrossRefGoogle ScholarPubMed
Okoth, J. O. and Kapaata, R. (1988). The hosts of Glossina fuscipes fuscipes (Newstead) in Busoga Uganda, and epidemiological implications for trypanosomiasis. Annals of Tropical Medicine and Parasitology 82, 517–518.CrossRefGoogle Scholar
Pepin, J. and Meda, H. A. (2001). The epidemiology and control of human African trypanosomiasis. Advances in Parasitology 49, 71–132.CrossRefGoogle ScholarPubMed
Ravel, S., Grébaut, P., Cuisance, D., and Cuny, G. (2003). Monitoring the developmental status of Trypanosoma brucei gambiense in the tsetse fly by means of PCR analysis of anal and saliva drops. Acta Tropica 88, 161–165.CrossRefGoogle ScholarPubMed
Ravel, S., Patrel, D., Koffi, M., Jamonneau, V. and Cuny, G. (2006). Cyclical transmission of Trypanosoma brucei gambiense in Glossina palpalis gambiensis displays great differences among field isolates. Acta Tropica 100, 151–155.CrossRefGoogle ScholarPubMed
Rio, R. V., Hu, Y. and Aksoy, S. (2004). Strategies of the home-team: symbioses exploited for vector-borne disease control. Trends in Microbiology 12, 325–333.CrossRefGoogle ScholarPubMed
Roberts, M. G. and Heesterbeek, J. A. P. (2003). A new method for estimating the effort required to control an infectious disease. Proceedings of the Royal Society of London, B 270, 1359–1364.CrossRefGoogle ScholarPubMed
Roditi, I. and Lehane, M. J. (2008). Interactions between trypanosomes and tsetse flies. Current Opinion in Microbiology 11, 345–351.CrossRefGoogle ScholarPubMed
Rogers, D. (1988). A general model for the African trypanosomiasis. Parsitology 97, 193–212.CrossRefGoogle Scholar
Rogers, D. and Randolph, S. (1991). Mortality rates and population density of tsetse flies correlated with satellite imagery. Nature, London 351, 739–741.CrossRefGoogle ScholarPubMed
Sanchez, M. A. and Blower, S. M. (1997). Uncertainty and sensitivity analysis of the basic reproductive rate. American Journal of Epidemiology 145, 1127–1137.CrossRefGoogle ScholarPubMed
Saltelli, A. (2002). Making the best use of model evaluations to compute sensitivity indices. Computer Physics Communication 145, 580–597.CrossRefGoogle Scholar
Saltelli, A., Tarantola, S., Campolongo, F. and Ratto, M. (2004) Sensitivity Analysis in Practice. John Wiley & Sons, Ltd, Chichester, UK.Google Scholar
Van den Bossche, P., Ky-Zerbo, A., Brandt, J., Marcotty, T., Geerts, S. and De Deken, R. (2005). Transmissibility of Trypanosoma brucei during its development in cattle. Tropical Medicine and International Health 10, 833–839.CrossRefGoogle ScholarPubMed
Waiswa, C., Picozzi, K., Katunguka-Rwakishaya, E., Olaho-Mukani, W., Musoke, R. A. and Welburn, S. C. (2006). Glossinga fuscipes fuscipes in the trypanosomiasis endemic areas of south eastern Uganda: Apparent density, trypanosome infection rates and host feeding preferences. Acta Tropica 99, 23–29.CrossRefGoogle ScholarPubMed
Welburn, S. C., Coleman, P. G., Maudlin, I., Fèvre, E. M., Odiit, M. and Eisler, M. C. (2006). Crisis, what crisis? Control of Rhodesian sleeping sickness. Trends in Parasitology 22, 123–128.CrossRefGoogle ScholarPubMed
Welburn, S. C., Fèvre, E. M., Coleman, P. G., Odiit, M. and Maudlin, I. (2001). Sleeping sickness: a tale of two diseases. Trends in Parasitology 17, 19–24.CrossRefGoogle ScholarPubMed
Welburn, S. C. and Maudlin, I. (1999). Tsetse-trypanosome interactions: rites of passage. Parasitology Today 15, 399–403.CrossRefGoogle ScholarPubMed
Welburn, S. C., Maudlin, I. and Milligan, P. J. M. (1995). Trypanozoon: infectivity to humans is linked to reduced transmissibility in tsetse I. Comparison of human serum resistant and human serum sensitive field isolates. Experimental Parasitology 81, 409–415.CrossRefGoogle ScholarPubMed
World Health Organization (2004). The World Health Report 2004. Changing History. World Health Organization, Geneva, Switzerland.Google Scholar