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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1999 Apr 29;354(1384):809–826. doi: 10.1098/rstb.1999.0433

Population biology of human onchocerciasis.

M G Basáñez 1, M Boussinesq 1
PMCID: PMC1692549  PMID: 10365406

Abstract

Human onchocerciasis (river blindness) is the filarial infection caused by Onchocerca volvulus and transmitted among people through the bites of the Simulium vector. Some 86 million people around the world are at risk of acquiring the nematode, with 18 million people infected and 600,000 visually impaired, half of them partially or totally blind. 99% of cases occur in tropical Africa; scattered foci exist in Latin America. Until recently control programmes, in operation since 1975, have consisted of antivectorial measures. With the introduction of ivermectin in 1988, safe and effective chemotherapy is now available. With the original Onchocerciasis Control Programme of West Africa coming to an end, both the new African Programme for Onchocerciasis Control and the Onchocerciasis Elimination Programme for the Americas, rely heavily on ivermectin self-sustained mass delivery. In consequence, the need for understanding the processes regulating parasite abundance in human and simuliid populations is of utmost importance. We present a simple mathematical framework built around recent analyses of exposure- and density-dependent processes operating, respectively, within the human and vector hosts. An expression for the basic reproductive ratio, R0, is derived and related to the minimum vector density required for parasite persistence in localities of West Africa in general and northern Cameroon in particular. Model outputs suggest that constraints acting against parasite establishment in both humans and vectors are necessary to reproduce field observations, but those in humans may not fully protect against reinfection. Analyses of host age-profiles of infection prevalence, intensity, and aggregation for increasing levels of endemicity and intensity of transmission in the Vina valley of northern Cameroon are in agreement with these results and discussed in light of novel work on onchocerciasis immunology.

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Selected References

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  1. Albiez E. J., Büttner D. W., Schulz-Key H. Studies on nodules and adult Onchocerca volvulus during a nodulectomy trial in hyperendemic villages in Liberia and Upper Volta. II. Comparison of the macrofilaria population in adult nodule carriers. Tropenmed Parasitol. 1984 Sep;35(3):163–166. [PubMed] [Google Scholar]
  2. Albiez E. J. Studies on nodules and adult Onchocerca volvulus during a nodulectomy trial in hyperendemic villages in Liberia and Upper Volta. I. Palpable and impalpable onchocercomata. Tropenmed Parasitol. 1983 Mar;34(1):54–60. [PubMed] [Google Scholar]
  3. Anderson J., Fuglsang H., Hamilton P. J., de Marshall T. F. Studies on onchocerciasis in the United Cameroon Republic. I. Comparison of populations with and without Onchocerca volvulus. Trans R Soc Trop Med Hyg. 1974;68(3):190–208. doi: 10.1016/0035-9203(74)90116-3. [DOI] [PubMed] [Google Scholar]
  4. Anderson J., Fuglsang H., Hamilton P. J., de Marshall T. F. Studies on onchocerciasis in the United Cameroon Republic. II. Comparison of onchocerciasis in rain-forest and Sudan-savanna. Trans R Soc Trop Med Hyg. 1974;68(3):209–222. doi: 10.1016/0035-9203(74)90117-5. [DOI] [PubMed] [Google Scholar]
  5. Anderson R. M., Gordon D. M. Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology. 1982 Oct;85(Pt 2):373–398. doi: 10.1017/s0031182000055347. [DOI] [PubMed] [Google Scholar]
  6. Anderson R. M., May R. M. Helminth infections of humans: mathematical models, population dynamics, and control. Adv Parasitol. 1985;24:1–101. doi: 10.1016/s0065-308x(08)60561-8. [DOI] [PubMed] [Google Scholar]
  7. Anderson R. M., May R. M. Herd immunity to helminth infection and implications for parasite control. Nature. 1985 Jun 6;315(6019):493–496. doi: 10.1038/315493a0. [DOI] [PubMed] [Google Scholar]
  8. Basáez M. G., Boussinesq M., Prod'hon J., Frontado H., Villamizar N. J., Medley G. F., Anderson R. M. Density-dependent processes in the transmission of human onchocerciasis: intensity of microfilariae in the skin and their uptake by the simuliid host. Parasitology. 1994 Jan;108(Pt 1):115–127. doi: 10.1017/s0031182000078586. [DOI] [PubMed] [Google Scholar]
  9. Basáez M. G., Remme J. H., Alley E. S., Bain O., Shelley A. J., Medley G. F., Anderson R. M. Density-dependent processes in the transmission of human onchocerciasis: relationship between the numbers of microfilariae ingested and successful larval development in the simuliid vector. Parasitology. 1995 May;110(Pt 4):409–427. doi: 10.1017/s0031182000064751. [DOI] [PubMed] [Google Scholar]
  10. Basáez M. G., Townson H., Williams J. R., Frontado H., Villamizar N. J., Anderson R. M. Density-dependent processes in the transmission of human onchocerciasis: relationship between microfilarial intake and mortality of the simuliid vector. Parasitology. 1996 Oct;113(Pt 4):331–355. doi: 10.1017/s003118200006649x. [DOI] [PubMed] [Google Scholar]
  11. Boussinesq M., Prod'hon J., Chippaux J. P. Onchocerca volvulus: striking decrease in transmission in the Vina valley (Cameroon) after eight annual large scale ivermectin treatments. Trans R Soc Trop Med Hyg. 1997 Jan-Feb;91(1):82–86. doi: 10.1016/s0035-9203(97)90406-5. [DOI] [PubMed] [Google Scholar]
  12. Bradley J. E., Elson L., Tree T. I., Stewart G., Guderian R., Calvopiña M., Paredes W., Araujo E., Nutman T. B. Resistance to Onchocerca volvulus: differential cellular and humoral responses to a recombinant antigen, OvMBP20/11. J Infect Dis. 1995 Sep;172(3):831–837. doi: 10.1093/infdis/172.3.831. [DOI] [PubMed] [Google Scholar]
  13. Cheke R. A., Garms R., Kerner M. The fecundity of Simulium damnosum s.l. in northern Togo and infections with Onchocerca spp. Ann Trop Med Parasitol. 1982 Oct;76(5):561–568. doi: 10.1080/00034983.1982.11687581. [DOI] [PubMed] [Google Scholar]
  14. Collins R. C., Brandling-Bennett A. D., Holliman R. B., Campbell C. C., Darsie R. F. Parasitological diagnosis of onchocerciasis: comparisons of incubation media and incubation times for skin snips. Am J Trop Med Hyg. 1980 Jan;29(1):35–41. doi: 10.4269/ajtmh.1980.29.35. [DOI] [PubMed] [Google Scholar]
  15. Das P. K., Manoharan A., Srividya A., Grenfell B. T., Bundy D. A., Vanamail P. Frequency distribution of Wuchereria bancrofti microfilariae in human populations and its relationships with age and sex. Parasitology. 1990 Dec;101(Pt 3):429–434. doi: 10.1017/s0031182000060625. [DOI] [PubMed] [Google Scholar]
  16. Davies J. B. Description of a computer model of forest onchocerciasis transmission and its application to field scenarios of vector control and chemotherapy. Ann Trop Med Parasitol. 1993 Feb;87(1):41–63. doi: 10.1080/00034983.1993.11812738. [DOI] [PubMed] [Google Scholar]
  17. Denham D. A., McGreevy P. B., Suswillo R. R., Rogers R. The resistance to re-infection of cats repeatedly inoculated with infective larvae of Brugia pahangi. Parasitology. 1983 Feb;86(Pt 1):11–18. doi: 10.1017/s0031182000057127. [DOI] [PubMed] [Google Scholar]
  18. Denham D. A., Ponnudurai T., Nelson G. S., Rogers R., Guy F. Studies with Brugia pahangi. II. The effect of repeated infection on parasite levels in cats. Int J Parasitol. 1972 Nov;2(4):401–407. doi: 10.1016/0020-7519(72)90084-7. [DOI] [PubMed] [Google Scholar]
  19. Disney R. H., Boreham P. F. Blood gorged resting blackflies in Cameroon and evidence of zoophily in Simulium damnosum. Trans R Soc Trop Med Hyg. 1969;63(2):286–287. doi: 10.1016/0035-9203(69)90163-1. [DOI] [PubMed] [Google Scholar]
  20. Duke B. O., Anderson J. A comparison of the lesions produced in the cornea of the rabbit eye by microfilariae of the forest and Sudan-savanna strains of Onchocerca volvulus from Cameroon. I. The clinical picture. Z Tropenmed Parasitol. 1972 Dec;23(4):354–368. [PubMed] [Google Scholar]
  21. Duke B. O., Anderson J., Fuglsang H. The Onchocerca volvulus transmission potentials and associated patterns of onchocerciasis at four Cameroon Sudan-savanna villages. Tropenmed Parasitol. 1975 Jun;26(2):143–154. [PubMed] [Google Scholar]
  22. Duke B. O. Human onchocerciasis--an overview of the disease. Acta Leiden. 1990;59(1-2):9–24. [PubMed] [Google Scholar]
  23. Duke B. O. Observations and reflections on the immature stages of Onchocerca volvulus in the human host. Ann Trop Med Parasitol. 1991 Feb;85(1):103–110. doi: 10.1080/00034983.1991.11812536. [DOI] [PubMed] [Google Scholar]
  24. Duke B. O. Observations on Onchocerca volvulus in experimentally infected chimpanzees. Tropenmed Parasitol. 1980 Mar;31(1):41–54. [PubMed] [Google Scholar]
  25. Duke B. O. Studies on factors influencing the transmission of onchocerciasis. 8. The escape of infective Onchocerca volvulus larvae from feeding 'forest' Simulium damnosum. Ann Trop Med Parasitol. 1973 Mar;67(1):95–99. doi: 10.1080/00034983.1973.11686866. [DOI] [PubMed] [Google Scholar]
  26. Duke B. O. Studies on factors influencing the transmisson of onchocerciasis. IV. The biting-cycles, infective biting density and transmission potential of "forest" Stimulium dannosum. Ann Trop Med Parasitol. 1968 Mar;62(1):95–106. doi: 10.1080/00034983.1968.11686535. [DOI] [PubMed] [Google Scholar]
  27. Duke B. O. The population dynamics of Onchocerca volvulus in the human host. Trop Med Parasitol. 1993 Jun;44(2):61–68. [PubMed] [Google Scholar]
  28. Eberhard M. L., Dickerson J. W., Boyer A. E., Tsang V. C., Zea-Flores R., Walker E. M., Richards F. O., Zea-Flores G., Strobert E. Experimental Onchocerca volvulus infections in mangabey monkeys (Cercocebus atys) compared to infections in humans and chimpanzees (Pan troglodytes). Am J Trop Med Hyg. 1991 Feb;44(2):151–160. doi: 10.4269/ajtmh.1991.44.151. [DOI] [PubMed] [Google Scholar]
  29. Elson L. H., Calvopiña M., Paredes W., Araujo E., Bradley J. E., Guderian R. H., Nutman T. B. Immunity to onchocerciasis: putative immune persons produce a Th1-like response to Onchocerca volvulus. J Infect Dis. 1995 Mar;171(3):652–658. doi: 10.1093/infdis/171.3.652. [DOI] [PubMed] [Google Scholar]
  30. Elson L. H., Days A., Calvopiña M., Paredes W., Araujo E., Guderian R. H., Bradley J. E., Nutman T. B. In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infect Immun. 1996 Dec;64(12):5061–5065. doi: 10.1128/iai.64.12.5061-5065.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Elson L. H., Guderian R. H., Araujo E., Bradley J. E., Days A., Nutman T. B. Immunity to onchocerciasis: identification of a putatively immune population in a hyperendemic area of Ecuador. J Infect Dis. 1994 Mar;169(3):588–594. doi: 10.1093/infdis/169.3.588. [DOI] [PubMed] [Google Scholar]
  32. Engelbrecht F., Schulz-Key H. Observations on adult Onchocerca volvulus maintained in vitro. Trans R Soc Trop Med Hyg. 1984;78(2):212–215. doi: 10.1016/0035-9203(84)90280-3. [DOI] [PubMed] [Google Scholar]
  33. Evans T. G. Socioeconomic consequences of blinding onchocerciasis in west Africa. Bull World Health Organ. 1995;73(4):495–506. [PMC free article] [PubMed] [Google Scholar]
  34. Finkelman F. D., Pearce E. J., Urban J. F., Jr, Sher A. Regulation and biological function of helminth-induced cytokine responses. Immunol Today. 1991 Mar;12(3):A62–A66. doi: 10.1016/S0167-5699(05)80018-0. [DOI] [PubMed] [Google Scholar]
  35. Finkelman F. D., Urban J. F., Jr Cytokines: making the right choice. Parasitol Today. 1992 Sep;8(9):311–314. doi: 10.1016/0169-4758(92)90105-b. [DOI] [PubMed] [Google Scholar]
  36. Fulford A. J., Butterworth A. E., Sturrock R. F., Ouma J. H. On the use of age-intensity data to detect immunity to parasitic infections, with special reference to Schistosoma mansoni in Kenya. Parasitology. 1992 Oct;105(Pt 2):219–227. doi: 10.1017/s003118200007414x. [DOI] [PubMed] [Google Scholar]
  37. Fulford A. J. Dispersion and bias: can we trust geometric means? Parasitol Today. 1994 Nov;10(11):446–448. doi: 10.1016/0169-4758(94)90181-3. [DOI] [PubMed] [Google Scholar]
  38. Gbakima A. A., Nutman T. B., Bradley J. E., McReynolds L. A., Winget M. D., Hong Y., Scott A. L. Immunoglobulin G subclass responses of children during infection with Onchocerca volvulus. Clin Diagn Lab Immunol. 1996 Jan;3(1):98–104. doi: 10.1128/cdli.3.1.98-104.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Gillespie A. J., Lustigman S., Rivas-Alcala A. R., Bradley J. E. The effect of ivermectin treatment on the antibody response to antigens of Onchocerca volvulus. Trans R Soc Trop Med Hyg. 1994 Jul-Aug;88(4):456–460. doi: 10.1016/0035-9203(94)90433-2. [DOI] [PubMed] [Google Scholar]
  40. Grenfell B. T., Michael E., Denham D. A. A model for the dynamics of human lymphatic filariasis. Parasitol Today. 1991 Nov;7(11):318–323. doi: 10.1016/0169-4758(91)90270-x. [DOI] [PubMed] [Google Scholar]
  41. Grenfell B. T., Michael E. Infection and disease in lymphatic filariasis: an epidemiological approach. Parasitology. 1992;104 (Suppl):S81–S90. doi: 10.1017/s0031182000075260. [DOI] [PubMed] [Google Scholar]
  42. Howe J. R., Lairmore T. C., Dou S., Mishra S. K., Dilley W. G., Donis-Keller H., Wells S. A., Jr Presymptomatic identification of carriers of the multiple endocrine neoplasia type 2A gene using flanking DNA markers. Surgery. 1992 Aug;112(2):219–226. [PubMed] [Google Scholar]
  43. Irvine M., Johnson E. H., Lustigman S. Identification of larval-stage-specific antigens of Onchocerca volvulus uniquely recognized by putative immune sera from humans and vaccination sera from animal models. Ann Trop Med Parasitol. 1997 Jan;91(1):67–77. doi: 10.1080/00034983.1997.11813113. [DOI] [PubMed] [Google Scholar]
  44. Kirkwood B., Smith P., Marshall T., Prost A. Relationships between mortality, visual acuity and microfilarial load in the area of the Onchocerciasis Control Programme. Trans R Soc Trop Med Hyg. 1983;77(6):862–868. doi: 10.1016/0035-9203(83)90308-5. [DOI] [PubMed] [Google Scholar]
  45. Kirkwood B., Smith P., Marshall T., Prost A. Variations in the prevalence and intensity of microfilarial infections by age, sex, place and time in the area of the Onchocerciasis Control Programme. Trans R Soc Trop Med Hyg. 1983;77(6):857–861. doi: 10.1016/0035-9203(83)90307-3. [DOI] [PubMed] [Google Scholar]
  46. LEBERRE R., BALAY G., BRENGUES J., COZ J. BIOLOGIE ET 'ECOLOGIE DE LA FEMELLE DE SIMULIUM DAMNOSUM THEOBALD, 1903, EN FONCTION DES ZONES BIOCLIMATIQUES D'AFRIQUE OCCIDENTALE. INFLUENCE SUR L''EPID'EMIOLOGIE DE L'ONCHOCERCOSE. Bull World Health Organ. 1964;31:843–855. [PMC free article] [PubMed] [Google Scholar]
  47. Maizels R. M., Bundy D. A., Selkirk M. E., Smith D. F., Anderson R. M. Immunological modulation and evasion by helminth parasites in human populations. Nature. 1993 Oct 28;365(6449):797–805. doi: 10.1038/365797a0. [DOI] [PubMed] [Google Scholar]
  48. Maizels R. M., Lawrence R. A. Immunological tolerance: The key feature in human filariasis? Parasitol Today. 1991 Oct;7(10):271–276. doi: 10.1016/0169-4758(91)90093-4. [DOI] [PubMed] [Google Scholar]
  49. Michael E., Bundy D. A. Herd immunity to filarial infection is a function of vector biting rate. Proc Biol Sci. 1998 May 22;265(1399):855–860. doi: 10.1098/rspb.1998.0370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Moreau J. P., Prost A., Prod'hon J. Essai de normalisation de la méthodologie des enquêtes clinco-parasitologiques sur l'onchocercose en Afrique de l'Ouest. Med Trop (Mars) 1978 Jan-Feb;38(1):43–51. [PubMed] [Google Scholar]
  51. Mosmann T. R., Moore K. W. The role of IL-10 in crossregulation of TH1 and TH2 responses. Immunol Today. 1991 Mar;12(3):A49–A53. doi: 10.1016/S0167-5699(05)80015-5. [DOI] [PubMed] [Google Scholar]
  52. Murdoch M. E., Hay R. J., Mackenzie C. D., Williams J. F., Ghalib H. W., Cousens S., Abiose A., Jones B. R. A clinical classification and grading system of the cutaneous changes in onchocerciasis. Br J Dermatol. 1993 Sep;129(3):260–269. doi: 10.1111/j.1365-2133.1993.tb11844.x. [DOI] [PubMed] [Google Scholar]
  53. Nwoke B. E. The socio-economic aspects of human onchocerciasis in Africa: present appraisal. J Hyg Epidemiol Microbiol Immunol. 1990;34(1):37–44. [PubMed] [Google Scholar]
  54. Pacala S. W., Dobson A. P. The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology. 1988 Feb;96(Pt 1):197–210. doi: 10.1017/s0031182000081762. [DOI] [PubMed] [Google Scholar]
  55. Plaisier A. P., van Oortmarssen G. J., Habbema J. D., Remme J., Alley E. S. ONCHOSIM: a model and computer simulation program for the transmission and control of onchocerciasis. Comput Methods Programs Biomed. 1990 Jan;31(1):43–56. doi: 10.1016/0169-2607(90)90030-d. [DOI] [PubMed] [Google Scholar]
  56. Plaisier A. P., van Oortmarssen G. J., Remme J., Habbema J. D. The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Trop. 1991 Feb;48(4):271–284. doi: 10.1016/0001-706x(91)90015-c. [DOI] [PubMed] [Google Scholar]
  57. Prost A., Gorim de Ponsay E. Importance épidémiologique du parasitisme neo-natal par microfilaires d'Onchocerca volvulus. Tropenmed Parasitol. 1979 Dec;30(4):477–481. [PubMed] [Google Scholar]
  58. Prost A., Hervouet J. P., Thylefors B. Les niveaux d'endémicité dans l'onchocercose. Bull World Health Organ. 1979;57(4):655–662. [PMC free article] [PubMed] [Google Scholar]
  59. Prost A., Prod'hon J. Le diagnostic parasitologique de l'onchocercose. Revue critique des methodes en usage. Med Trop (Mars) 1978 Sep-Oct;38(5):519–532. [PubMed] [Google Scholar]
  60. Prost A. The burden of blindness in adult males in the savanna villages of West Africa exposed to onchocerciasis. Trans R Soc Trop Med Hyg. 1986;80(4):525–527. doi: 10.1016/0035-9203(86)90129-x. [DOI] [PubMed] [Google Scholar]
  61. Prost A., Vaugelade J. La surmortalité des aveugles en zone de savane ouest-africaine. Bull World Health Organ. 1981;59(5):773–776. [PMC free article] [PubMed] [Google Scholar]
  62. Remme J., Ba O., Dadzie K. Y., Karam M. 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. Bull World Health Organ. 1986;64(5):667–681. [PMC free article] [PubMed] [Google Scholar]
  63. Renz A., Fuglsang H., Anderson J. 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. Ann Trop Med Parasitol. 1987 Jun;81(3):253–262. doi: 10.1080/00034983.1987.11812118. [DOI] [PubMed] [Google Scholar]
  64. Renz A. 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. Ann Trop Med Parasitol. 1987 Jun;81(3):239–252. doi: 10.1080/00034983.1987.11812117. [DOI] [PubMed] [Google Scholar]
  65. Renz A., Wenk P., Anderson J., Fuglsang H. Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon V. What is a tolerable level of Annual Transmission Potential? Ann Trop Med Parasitol. 1987 Jun;81(3):263–274. doi: 10.1080/00034983.1987.11812119. [DOI] [PubMed] [Google Scholar]
  66. Renz A., Wenk P. Studies on the dynamics of transmission of onchocerciasis in a Sudan-savanna area of North Cameroon I. Prevailing Simulium vectors, their biting rates and age-composition at different distances from their breeding sites. Ann Trop Med Parasitol. 1987 Jun;81(3):215–228. doi: 10.1080/00034983.1987.11812115. [DOI] [PubMed] [Google Scholar]
  67. Schulz-Key H., Karam M. Periodic reproduction of Onchocerca volvulus. Parasitol Today. 1986 Oct;2(10):284–286. doi: 10.1016/0169-4758(86)90138-9. [DOI] [PubMed] [Google Scholar]
  68. Schulz-Key H. Observations on the reproductive biology of Onchocerca volvulus. Acta Leiden. 1990;59(1-2):27–44. [PubMed] [Google Scholar]
  69. Schulz-Key H., Soboslay P. T., Hoffmann W. H. Ivermectin-facilitated immunity. Parasitol Today. 1992 May;8(5):152–153. doi: 10.1016/0169-4758(92)90003-k. [DOI] [PubMed] [Google Scholar]
  70. Schweitzer A. N., Anderson R. M. The regulation of immunological responses to parasitic infections and the development of tolerance. Proc Biol Sci. 1992 Feb 22;247(1319):107–112. doi: 10.1098/rspb.1992.0015. [DOI] [PubMed] [Google Scholar]
  71. Scott M. E. Temporal changes in aggregation: a laboratory study. Parasitology. 1987 Jun;94(Pt 3):583–595. doi: 10.1017/s0031182000055918. [DOI] [PubMed] [Google Scholar]
  72. Shelley A. J. Simuliidae and the transmission and control of human Onchocerciasis in Latin America. Cad Saude Publica. 2005 Mar 28;7(3):310–327. doi: 10.1590/s0102-311x1991000300003. [DOI] [PubMed] [Google Scholar]
  73. Soboslay P. T., Dreweck C. M., Hoffmann W. H., Lüder C. G., Heuschkel C., Görgen H., Banla M., Schulz-Key H. Ivermectin-facilitated immunity in onchocerciasis. Reversal of lymphocytopenia, cellular anergy and deficient cytokine production after single treatment. Clin Exp Immunol. 1992 Sep;89(3):407–413. doi: 10.1111/j.1365-2249.1992.tb06971.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Soboslay P. T., Dreweck C. M., Taylor H. R., Brotman B., Wenk P., Greene B. M. Experimental onchocerciasis in chimpanzees. Cell-mediated immune responses, and production and effects of IL-1 and IL-2 with Onchocerca volvulus infection. J Immunol. 1991 Jul 1;147(1):346–353. [PubMed] [Google Scholar]
  75. Stewart G. R., Elson L., Araujo E., Guderian R., Nutman T. B., Bradley J. E. Isotype-specific characterization of antibody responses to Onchocerca volvulus in putatively immune individuals. Parasite Immunol. 1995 Jul;17(7):371–380. doi: 10.1111/j.1365-3024.1995.tb00904.x. [DOI] [PubMed] [Google Scholar]
  76. Tada I., Aoki Y., Rimola C. E., Ikeda T., Matsuo K., Ochoa J. O., Recinos M., Sato S., Godoy H. A., Orellana J. J. Onchocerciasis in San Vicente Pacaya, Guatemala. Am J Trop Med Hyg. 1979 Jan;28(1):67–71. doi: 10.4269/ajtmh.1979.28.67. [DOI] [PubMed] [Google Scholar]
  77. Thylefors B., Philippon B., Prost A. Transmission potentials of Onchocerca volvulus and the associated intensity of onchocerciasis in a Sudan-savanna area. Tropenmed Parasitol. 1978 Sep;29(3):346–354. [PubMed] [Google Scholar]
  78. Toe L., Merriweather A., Unnasch T. R. DNA probe-based classification of Simulium damnosum s. l.-borne and human-derived filarial parasites in the onchocerciasis control program area. Am J Trop Med Hyg. 1994 Nov;51(5):676–683. [PubMed] [Google Scholar]
  79. Trees A. J. Onchocerca ochengi: Mimic, model or modulator of O. volvulus? Parasitol Today. 1992 Oct;8(10):337–339. doi: 10.1016/0169-4758(92)90068-d. [DOI] [PubMed] [Google Scholar]
  80. Trees A. J., Wahl G., Kläger S., Renz A. Age-related differences in parasitosis may indicate acquired immunity against microfilariae in cattle naturally infected with Onchocerca ochengi. Parasitology. 1992 Apr;104(Pt 2):247–252. doi: 10.1017/s0031182000061680. [DOI] [PubMed] [Google Scholar]
  81. Vanamail P., Subramanian S., Das P. K., Pani S. P., Rajagopalan P. K., Bundy D. A., Grenfell B. T. Estimation of age-specific rates of acquisition and loss of Wuchereria bancrofti infection. Trans R Soc Trop Med Hyg. 1989 Sep-Oct;83(5):689–693. doi: 10.1016/0035-9203(89)90399-4. [DOI] [PubMed] [Google Scholar]
  82. Wada Y. Theoretical approach to the epidemiology of onchocerciasis in Guatemala. Jpn J Med Sci Biol. 1982 Aug;35(4):183–196. doi: 10.7883/yoken1952.35.183. [DOI] [PubMed] [Google Scholar]
  83. Walsh J. F., Davies J. B., Le Berre R., Grams R. Standardization of criteria for assessing the effect of Simulium control in onchocerciasis control programmes. Trans R Soc Trop Med Hyg. 1978;72(6):675–676. doi: 10.1016/0035-9203(78)90039-1. [DOI] [PubMed] [Google Scholar]
  84. Woolhouse M. E., Ndamba J., Bradley D. J. The interpretation of intensity and aggregation data for infections of Schistosoma haematobium. Trans R Soc Trop Med Hyg. 1994 Sep-Oct;88(5):520–526. doi: 10.1016/0035-9203(94)90144-9. [DOI] [PubMed] [Google Scholar]
  85. Woolhouse M. E., Taylor P., Matanhire D., Chandiwana S. K. Acquired immunity and epidemiology of Schistosoma haematobium. Nature. 1991 Jun 27;351(6329):757–759. doi: 10.1038/351757a0. [DOI] [PubMed] [Google Scholar]
  86. Zimmerman P. A., Dadzie K. Y., De Sole G., Remme J., Alley E. S., Unnasch T. R. Onchocerca volvulus DNA probe classification correlates with epidemiologic patterns of blindness. J Infect Dis. 1992 May;165(5):964–968. doi: 10.1093/infdis/165.5.964. [DOI] [PubMed] [Google Scholar]

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