Human infection patterns and heterogeneous exposure in river blindness.

Here we analyze patterns of human infection with Onchocerca volvulus (the cause of river blindness) in different continents and ecologies. In contrast with some geohelminths and schistosome parasites whose worm burdens typically exhibit a humped pattern with host age, patterns of O. volvulus infection vary markedly with locality. To test the hypothesis that such differences are partly due to heterogeneity in exposure to vector bites, we develop an age- and sex-structured model for intensity of infection, with parasite regulation within humans and vectors. The model is fitted to microfilarial data from savannah villages of northern Cameroon, coffee fincas of central Guatemala, and forest-dwelling communities of southern Venezuela that were recorded before introducing ivermectin treatment. Estimates of transmission and infection loads are compared with entomological and epidemiological field data. Host age- and sex-heterogeneous exposure largely explains locale-specific infection patterns in onchocerciasis (whereas acquired protective immunity has been invoked for other helminth infections). The basic reproductive number, R0, ranges from 5 to 8, which is slightly above estimates for other helminth parasites but well below previously presented values.

[1]  María-Gloria Basáñez,et al.  Human Onchocerciasis in the Amazonian Area of Southern Venezuela: Spatial and Temporal Variations in Biting and Parity Rates of Black Fly (Diptera: Simuliidae) Vectors , 2001, Journal of medical entomology.

[2]  K. Dietz,et al.  Density-dependent parasite establishment suggests infection-associated immunosuppression as an important mechanism for parasite density regulation in onchocerciasis. , 2003, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[3]  M. Martcheva Exponential growth in age-structured two-sex populations. , 1999, Mathematical biosciences.

[4]  M. Basáñez,et al.  Onchocerciasis hyperendemic in the Unturán Mountains: the value of recombinant antigens in describing a new transmission area in southern Venezuela. , 1999, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[5]  M. Little,et al.  Transmission intensity and the patterns of Onchocerca volvulus infection in human communities. , 2002, The American journal of tropical medicine and hygiene.

[6]  M. Woolhouse,et al.  Acquired immunity and epidemiology of Schistosoma haematobium , 1991, Nature.

[7]  Max Sussman,et al.  Topley and Wilson's Microbiology and Microbial infections , 1998 .

[8]  R. Collins,et al.  Onchocerciasis in Guatemala. Epidemiology in fincas with various intensities of infection. , 1981, The American journal of tropical medicine and hygiene.

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

[10]  K. Dietz,et al.  On the interpretation of age–intensity profiles and dispersion patterns in parasitological surveys , 2003, Parasitology.

[11]  M. Grillet,et al.  Onchocerciasis in the Amazonian focus of southern Venezuela: altitude and blackfly species composition as predictors of endemicity to select communities for ivermectin control programmes. , 1998, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[12]  J. M. Elliott,et al.  Some methods for the statistical analysis of samples of benthic invertebrates , 1971 .

[13]  T. Marshall,et al.  Studies on onchocerciasis in the United Cameroon Republic. II. Comparison of onchocerciasis in rain-forest and Sudan-savanna. , 1974, Transactions of the Royal Society of Tropical Medicine and Hygiene.

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

[15]  M. Basáñez,et al.  Association between microfilarial load and excess mortality in onchocerciasis: an epidemiological study , 2004, The Lancet.

[16]  R. Tibshirani,et al.  An Introduction to the Bootstrap , 1995 .

[17]  H. Fuglsang,et al.  Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon IV. The different exposure to Simulium bites and transmission of boys and girls and men and women, and the resulting manifestations of onchocerciasis. , 1987, Annals of tropical medicine and parasitology.

[18]  Robert Tibshirani,et al.  An Introduction to the Bootstrap CHAPMAN & HALL/CRC , 1993 .

[19]  C. Cosner,et al.  Models for the effects of individual size and spatial scale on competition between species in heterogeneous environments. , 1995, Mathematical biosciences.

[20]  B. Duke The population dynamics of Onchocerca volvulus in the human host. , 1993, Tropical medicine and parasitology : official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit.

[21]  M. Boussinesq,et al.  Onchocerca volvulus: striking decrease in transmission in the Vina valley (Cameroon) after eight annual large scale ivermectin treatments. , 1997, Transactions of the Royal Society of Tropical Medicine and Hygiene.

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

[23]  A. Renz Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon III. Infection rates of the Simulium vectors and Onchocerca volvulus transmission potentials. , 1987, Annals of tropical medicine and parasitology.

[24]  B. Kirkwood,et al.  Variations in the prevalence and intensity of microfilarial infections by age, sex, place and time in the area of the Onchocerciasis Control Programme. , 1983, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[25]  Y. Wada Theoretical approach to the epidemiology of onchocerciasis in Guatemala. , 1982, Japanese journal of medical science & biology.

[26]  J. Remmé,et al.  A force-of-infection model for onchocerciasis and its applications in the epidemiological evaluation of the Onchocerciasis Control Programme in the Volta River basin area. , 1986, Bulletin of the World Health Organization.

[27]  Peter J. Hudson,et al.  The ecology of wildlife diseases , 2002 .

[28]  L. Brabin Factors affecting the differential susceptibility of males and females to onchocerciasis. , 1990, Acta Leidensia.

[29]  I. Tada,et al.  Onchocerciasis in San Vicente Pacaya, Guatemala. , 1979, The American journal of tropical medicine and hygiene.

[30]  J D Habbema,et al.  ONCHOSIM: a model and computer simulation program for the transmission and control of onchocerciasis. , 1990, Computer methods and programs in biomedicine.

[31]  M. Boussinesq,et al.  Population biology of human onchocerciasis. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  K. Dietz,et al.  The relationships between the burden of adult parasites, host age and the microfilarial density in human onchocerciasis. , 2004, International journal for parasitology.

[33]  J. B. Davies Description of a computer model of forest onchocerciasis transmission and its application to field scenarios of vector control and chemotherapy. , 1993, Annals of tropical medicine and parasitology.

[34]  A. Prost [Latency period in onchocerciasis]. , 1980, Bulletin of the World Health Organization.

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

[36]  M. Basáñez,et al.  Density dependence and the control of helminth parasites. , 2006, The Journal of animal ecology.

[37]  R. M. May,et al.  Herd immunity to helminth infection and implications for parasite control , 1985, Nature.