Chapter 11 Onchocerca-Simulium Interactions and the Population and Evolutionary Biology of Onchocerca volvulus

Advances in Parasitology

Volumn 68, Issue , 2009, Pages 263-313

  Basáñez, María Gloria ^a,c   Churcher, Thomas S ^a   Grillet, María Eugenia ^b,c,d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^c University of Toronto ^*

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHELMINTIC AGENT; IVERMECTIN;

AFRICA; DISEASE TRANSMISSION; ENDEMIC DISEASE; EVOLUTION; HOST PARASITE INTERACTION; HUMAN; LIFE CYCLE; MICROFILARIA (NEMATODE LARVA); MICROFILARIASIS; NONHUMAN; ONCHOCERCA VOLVULUS; ONCHOCERCIASIS; PARASITE CONTROL; PARASITE DEVELOPMENT; PARASITE SURVIVAL; POPULATION BIOLOGY; POPULATION DYNAMICS; PRIORITY JOURNAL; RESERVOIR; REVIEW; SIMULIUM; SOUTH AND CENTRAL AMERICA; ZOONOSIS; ANIMAL; FLY; GENETICS; PARASITOLOGY; PHYSIOLOGY;

ONCHOCERCA; ONCHOCERCA VOLVULUS; SIMULIIDAE;

ANIMALS; EVOLUTION; HOST-PARASITE INTERACTIONS; HUMANS; ONCHOCERCA VOLVULUS; ONCHOCERCIASIS; SIMULIIDAE;

EID: 61849096677     PISSN: 0065308X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-308X(08)00611-8     Document Type: Review

References (152)

1. Andrade B.B., Teixeira C.R., Barral A., and Barral-Netto M. Haematophagous arthropod saliva and host defense system: A tale of tear and blood. Ann. Braz. Acad. Sci. 77 (2005) 665-693
2. Anscombe F.J. The transformation of Poisson, binomial and negative-binomial data. Biometrika 35 (1948) 246-254
3. Awadzi K., Attah S.K., Addy E.T., Opoku N.O., Quartey B.T., Lazdins-Helds J.K., Ahmed K., Boatin B.A., Boakye D.A., and Edwards G. Thirty-month follow-up of sub-optimal responders to multiple treatments with ivermectin, in two onchocerciasis-endemic foci in Ghana. Ann. Trop. Med. Parasitol. 98 (2004) 359-370
4. Awadzi K., Boakye D.A., Edwards G., Opoku N.O., Attah S.K., Osei-Atweneboana M.Y., Lazdins-Helds J.K., Ardrey A.E., Addy E.T., Quartey B.T., Ahmed K., Boatin B.A., and Soumbey-Alley E.W. An investigation of persistent microfilaridermias despite multiple treatments with ivermectin, in two onchocerciasis-endemic foci in Ghana. Ann. Trop. Med. Parasitol. 98 (2004) 231-249
5. Ayesta C., Basáñez M.G., Ramí-rez-Pérez J., Peceño C., Aldana E., Botto C., and Narbaiza I. Estudio del aparato bucal de Simulium pintoi mediante microscopí-a electrónica de barrido. In: Yarźbal L., Botto C., and Allan R. (Eds). La Oncocercosis en América (1985), Ediciones CAICET, Caracas 87-96 Publ. Cient. No. 3
6. Bain O. Le genre Onchocerca: Hypothèses sur son évolution et clé dichotomique des espèces. Ann. Parasitol. Hum. Comp. 56 (1981) 503-526
7. Bain O., Durette Desset M.C., and De León J.R. Onchocercose au Guatemala: l'ingestion des microfilaires par Simulium ochraceum et leur passage dans l'hémocèle de ce vecteur. Ann. Parasitol. Hum. Comp. 49 (1974) 467-487
8. Bain O., Philippon B., Séchan Y., and Cassone J. Corrélation entre le nombre de microfilaires ingérées et l'épaisseur de la membrane péritrophique du vecteur dans l'onchocercose de savane africaine. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 283 (1976) 391-392
9. Bain O., Vuong P., Petit G., Prod'hon J., Ranque P., and Chabaud A.G. Différences dans la localisation des microfilaires d'O. volvulus en savane et en forêt: implications cliniques éventuelles. Ann. Parasitol. Hum. Comp. 61 (1986) 125-126
10. Basáñez M.G., and Ricárdez-Esquinca J. Models for the population biology and control of human onchocerciasis. Trends Parasitol. 17 (2001) 430-438
11. Basáñez M.G., Boussinesq M., Prod'hon J., Frontado H., Villamizar N.J., Medley G.F., and 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 108 (1994) 115-127
12. Basáñez M.G., Collins R.C., Porter C.H., Little M.P., and Brandling-Bennett D. Transmission intensity and the patterns of Onchocerca volvulus infection in human communities. Am. J. Trop. Med. Hyg. 67 (2002) 669-679
13. Basáñez M.G., Pion S.D.S., Boakes E., Filipe J.A.N., Churcher T.S., and Boussinesq M. Effect of single dose ivermectin on Onchocerca volvulus: A systematic review and meta-analysis. Lancet Infect. Dis. 8 (2008) 310-322
14. Basáñez M.G., Pion S.D.S., Churcher T.S., Breitling L., Little M.P., and Boussinesq M. River blindness: A success story under threat?. PLoS Med. 3 (2006) e371
15. Basáñez M.G., Razali K., Renz A., and Kelly D. Density-dependent host choice by disease vectors: Epidemiological implications of the ideal free distribution. Trans. R. Soc. Trop. Med. Hyg. 101 (2007) 256-269
16. Basáñez M.G., Remme J.H.F., Alley E.S., Bain O., Shelley A.J., Medley G.F., and 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 110 (1995) 409-427
17. Basáñez M.G., Townson H., Williams J.R., Frontado H., Villamizar N.J., and Anderson R.M. Density-dependent processes in the transmission of human onchocerciasis: Relationship between microfilarial intake and mortality of the simuliid vector. Parasitology 113 (1996) 331-355
18. Basáñez M.G., Yarzábal L., Frontado H.L., and Villamizar N.J. Onchocerca-Simulium complexes in Venezuela: Can human onchocerciasis spread outside its present endemic areas?. Parasitology 120 (2000) 143-160
19. Boakye D.A. A pictorial guide to the chromosomal identification of members of the Simulium damnosum Theobald complex in West Africa with particular reference to the Onchocerciasis Control Programme area. Trop. Med. Parasitol. 44 (1993) 223-244
20. Boakye D.A., and Meredith S.E.O. Introgression between members of the Simulium damnosum complex: Larvicidal implications. Med. Vet. Entomol. 7 (1993) 393-397
21. Boakye D.A., and Mosha F.W. Natural hybridization between Simulium sanctipauli and S. sirbanum, two sibling species of the S. damnosum complex. Med. Vet. Entomol. 2 (1988) 397-399
22. Boakye D.A., Back C., and Brakefield P.M. Evidence of multiple mating and hybridization in Simulium damnosum s.l. (Diptera: Simuliidae) in nature. J. Med. Entomol. 37 (2000) 29-34
23. Boakye D.A., Back C., Fiasorgbor G.K., Sib A.P., and Coulibaly Y. Sibling species distributions of the Simulium damnosum complex in the west African Onchocerciasis Control Programme area during the decade 1984-93, following intensive larviciding since 1974. Med. Vet. Entomol. 12 (1998) 345-358
24. Bottomley C., Isham V., Collins R.C., and Basáñez M.G. Rates of microfilarial production by Onchocerca volvulus are not cumulatively reduced by multiple ivermectin treatments. Parasitology 135 (2008) 1571-1581
25. Boussinesq M. Etude épidémiologique de l'onchocercose en zone de savane camerounaise. Effets d'un traitement de masse par l'ivermectine (1991), Ph.D. Thesis. University of Montpellier II, France
26. Brandling-Bennett A.D., and Darsie R.F. Distribution of microfilariae in Guatemalans with onchocerciasis. Trans. R. Soc. Trop. Med. Hyg. 77 (1983) 254-258
27. Campbell C.C., Collins R.C., Huong A.Y., and Figueroa Marroquin H. Quantitative aspects of the infection of Simulium ochraceum by Onchocerca volvulus: The relation of skin microfilarial density to vector infection. Tropenmed. Parasitol. 31 (1980) 475-478
28. Carroll R.J., Ruppert D., and Stefanski L.A. Measurement Error in Nonlinear Models (1995), Chapman and Hall, London
29. Charalambous M., Shelley A.J., and Arzube M. The potential for dispersal of onchocerciasis in Ecuador in relation to the distribution of the vector Simulium exiguum (Diptera: Simuliidae). Mem. Inst. Oswaldo Cruz 92 (1997) 153-156
30. Cheke R.A., Garms R., and Kerner M. The fecundity of Simulium damnosum s.l. in northern Togo and infections with Onchocerca spp. Ann. Trop. Med. Parasitol. 76 (1982) 561-568
31. Churcher T.S., and Basáñez M.G. Density dependence and the spread of anthelmintic resistance. Evolution 62 (2008) 528-537
32. Churcher T.S., and Basáñez M.G. Sampling strategies to detect anthelmintic resistance: The perspective of human onchocerciasis. Trends Parasitol 25 (2008) 11-17 Nov. 11, 2008 [Epub ahead of print]. Printed in 2009 as
33. Churcher T.S., Ferguson N.M., and Basáñez M.G. Density dependence and overdispersion in the transmission of helminth parasites. Parasitology 131 (2005) 121-132
34. Churcher T.S., Filipe J.A.N., and Basáñez M.G. Density dependence and the control of helminth parasites. J. Animal Ecol. 75 (2006) 1313-1320
35. Collins R.C., Campbell C.C., Wilton D.P., and Newton L. Quantitative aspects of the infection of Simulium ochraceum by Onchocerca volvulus. Tropenmed. Parasitol. 28 (1977) 235-243
36. Collins R.C., Lehmann T., Vieira G.,J.C., and Guderian R.H. Vector competence of Simulium exiguum for Onchocerca volvulus: Implications for the epidemiology of onchocerciasis. Am. J. Trop. Med. Hyg. 52 (1995) 213-218
37. Cupp E., Richards F., Lammie P., and Eberhard M. Efficacy of ivermectin against Onchocerca volvulus in Ghana. Correspondence apropos Osei-Atweneboana et al. (2007). Lancet 370 (2007) 1123
38. Cupp E.W., and Cupp M.S. Black fly (Diptera: Simuliidae) salivary secretions: Importance in vector competence and disease. J. Med. Entomol. 34 (1997) 87-94
39. Cupp E.W., and Cupp M.S. Impact of ivermectin community-level treatments on elimination of adult Onchocerca volvulus when individuals receive multiple treatments per year. Am. J. Trop. Med. Hyg. 73 (2005) 1159-1161
40. Cupp M.S., Cupp E.W., Ochoa J.O., and Moulton J.K. Salivary apyrase in New World blackflies (Diptera: Simuliidae) and its relationship to onchocerciasis vector status. Med. Vet. Entomol. 9 (1995) 325-330
41. Dalmat H.T. The Blackflies (Diptera: Simuliidae) of Guatemala and their Role as Vectors of Onchocerciasis (1955), Smithsonian Miscellaneous Collection 125 Smithsonian Institute, Washington
42. De Leon J.R., and Duke B.O.L. Experimental studies on the transmission of Guatemalan and West African strains of Onchocerca volvulus by Simulium ochraceum, S. metallicum and S. callidum. Trans. R. Soc. Trop. Med. Hyg. 60 (1966) 735-752
43. Demanou M., Enyong P., Pion S.D.S., Basáñez M.G., and Boussinesq M. Experimental studies on the transmission of Onchocerca volvulus by its vector in the Sanaga valley (Cameroon): Simulium squamosum B. Intake of microfilariae and their migration to the haemocoel of the vector. Ann. Trop. Med. Parasitol. 97 (2003) 381-402
44. Duerr H.P., Dietz K., and Eichner M. Determinants of the eradicability of filarial infections: A conceptual approach. Trends Parasitol. 21 (2005) 88-96
45. Duerr H.P., Dietz K., Schulz-Key H., Büttner D.W., and Eichner M. Density-dependent parasite establishment suggests infection-associated immunosuppression as an important mechanism for parasite density regulation in onchocerciasis. Trans. R. Soc. Trop. Med. Hyg. 97 (2003) 242-250
46. Duerr H.P., Hoffmann W.H., and Eichner M. Does resistance to filarial reinfections become leaky over time?. Trends Parasitol. 24 (2008) 350-354
47. Duerr H.P., Leary C.C., and Eichner M. High infection rates at low transmission potentials in West African onchocerciasis. Int. J. Parasitol. 36 (2006) 1367-1372
48. Duke B.O.L. Studies on factors influencing the transmission of onchocerciasis. II. The intake of Onchocerca volvulus microfilariae by Simulium damnosum and the survival of the parasites in the fly under laboratory conditions. Ann. Trop. Med. Parasitol. 56 (1962) 255-263
49. Duke B.O.L. Studies on factors influencing the transmission of onchocerciasis. VI. The infective biting potential of Simulium damnosum in different bioclimatic zones and its influence on the transmission potential. Ann. Trop. Med. Parasitol. 62 (1968) 164-170
50. Duke B.O.L. Onchocerca-Simulium complexes. VI. Experimental studies on the transmission of Venezuelan and West African strains of Onchocerca volvulus by Simulium metallicum and S. exiguum in Venezuela. Ann. Trop. Med. Parasitol. 64 (1970) 421-431
51. Duke B.O.L., Lewis D.J., and Moore P.J. Onchocerca-Simulium complexes. I. Transmission of forest and Sudan-savanna strains of Onchocerca volvulus from Cameroon by Simulium damnosum from various West African bioclimatic zones. Ann. Trop. Med. Parasitol. 60 (1966) 318-336
52. Duke B.O.L., Moore P.J., and De Leon J.R. Onchocerca-Simulium complexes. V. The intake and subsequent fate of a Guatemalan strain of Onchocerca volvulus in forest and Sudan-savanna forms of West African Simulium damnosum. Ann. Trop. Med. Parasitol. 61 (1967) 332-337
53. Failloux A.B., Raymond M., Ung A., Glaziou P., Martin P.M.V., and Pasteur N. Variation in the vector competence of Aedes polynesiensis for Wuchereria bancrofti. Parasitology 111 (1995) 19-29
54. Filipe J.A.N., Boussinesq M., Renz A., Collins R.C., Vivas-Martinez S., Grillet M.E., Little M.P., and Basáñez M.G. Human infection patterns and heterogeneous exposure in river blindness. Proc. Natl. Acad. Sci. USA 102 (2005) 15265-15270
55. Gambhir M., and Michael E. Complex ecological dynamics and eradicability of the vector borne macroparasitic disease, lymphatic filariasis. PLoS One 3 (2008) e2874
56. Grillet M.E., Basáñez M.G., Vivas-Martínez S., Villamizar N., Frontado H., Cortez J., Coronel P., and Botto C. Human onchocerciasis in the Amazonian area of southern Venezuela: Spatial and temporal variations in biting and parity rates of black fly (Diptera: Simuliidae) vectors. J. Med. Entomol. 38 (2001) 520-530
57. Grillet M.E., Botto C., Basáñez M.G., and Barrera R. Vector competence of Simulium metallicum s.l. (Diptera: Simuliidae) in two endemic areas of human onchocerciasis in northern Venezuela. Ann. Trop. Med. Parasitol. 88 (1994) 65-75
58. Grillet M.E., Villamizar N.J., Frontado H.L., Cortez J., Escalona M., Botto C., and Basáñez M.G. Vector competence of Simulium oyapockense s.l. and S. incrustatum for Onchocerca volvulus: Implications for ivermectin-based control in the Amazonian focus of human onchocerciasis, a multi-vector-host system. Acta Trop. 107 (2008) 80-89
59. Guderian R.H., and Shelley A.J. Onchocerciasis in Ecuador: The situation in 1989. Mem. Inst. Oswaldo Cruz 87 (1992) 405-415
60. Hagen H.E., and Kläger S.L. Integrin-like RGD-dependent cell adhesion mechanism is involved in the rapid killing of Onchocerca microfilariae during early infection of Simulium damnosum s.l. Parasitology 122 (2001) 433-438
61. Hagen H.E., Kläger S.L., Barrault D.V., and Ham P.J. The effects of protease inhibitors and sugars on the survival and development of the parasite Onchocerca ochengi in its natural intermediate host Simulium damnosum s.l. Trop. Med. Int. Health 2 (1997) 211-217
62. Hagen H.E., Kläger S.L., Chan V., Sakanari J.A., McKerrow J.H., and Ham P.J. Simulium damnosum s.l.: Identification of inducible serine proteases following an Onchocerca infection by differential display reverse transcription PCR. Exp. Parasitol. 8 (1995) 249-254
63. Hagen H.E., Kläger S.L., McKerrow J.H., and Ham P.J. Simulium damnosum s.l.: Isolation and identification of prophenoloxidase following an infection with Onchocerca spp. using targeted differential display. Exp. Parasitol. 86 (1997) 213-218
64. Ham P.J. Acquired resistance to Onchocerca lienalis infections in Simulium ornatum Meigen and Simulium lineatum Meigen following passive transfer of haemolymph from previously infected simuliids (Diptera: Simuliidae). Parasitology 92 (1986) 269-277
65. Ham P.J., and Banya A.J. The effect of experimental Onchocerca infections on the fecundity and oviposition of laboratory reared Simulium sp. (Diptera, Simuliidae). Tropenmed. Parasitol. 35 (1984) 61-66
66. Ham P.J., Albuquerque C., Baxter A.J., Chalk R., and Hagen H.E. Humoral immune responses in blackfly and mosquito vectors of filariae. In: Approaches to vector control: new and trusted. Trans. R. Soc. Trop. Med. Hyg. 88 (1994) 132-135
67. Ham P.J., Baxter A.J., Thomas P.M., Phillips L., and Townson H. Resistance to reinfection of Simulium with Onchocerca and potential mechanisms for control. Acta Leiden. 59 (1990) 151-152
68. Higazi T.B., Filiano A., Katholi C.R., Dadzie Y., Remme J.H., and Unnasch T.R. Wolbachia endosymbiont levels in severe and mild strains of Onchocerca volvulus. Mol. Biochem. Parasitol. 141 (2005) 109-112
69. Hurd H. Manipulation of medically important insect vectors by their parasites. Annu. Rev. Entomol. 48 (2003) 141-161
70. Jerwood D., Lewis T., and Saporu F.W.O. Modelling the migration of Onchocerca volvulus in simuliids using a simple compartmental process. Biometrics 40 (1984) 313-322
71. Kawabata M., Hashiguchi Y., Zea G., Yamada H., Aoki Y., Tada I., Recinos M.M., and Flores O. The distribution of microfilariae in the skin of Guatemalan onchocerciasis patients: An evaluation of diagnostic potentials. J. Helminthol. 54 (1980) 183-190
72. Kershaw W.E., Duke B.O.L., and Budden F.H. Distribution of microfilariae of O. volvulus in the skin. Its relation to the skin changes and to eye lesions and blindness. Br. Med. J. 2 (1954) 724-729
73. Kirkwood B.R., and Sterne A.C. "Essential Medical Statistics" second ed. Blackwell Science, Oxford (2003)
74. Kläger S.L., Hagen H.E., and Bradley J.E. Effects of an Onchocerca-derived cysteine protease inhibitor on microfilariae in their simuliid vector. Parasitology 118 (1999) 305-310
75. Kläger S.L., Watson A., Achukwi D., Hultmark D., and Hagen H.E. Humoral immune response of Simulium damnosum s.l. following filarial and bacterial infections. Parasitology 125 (2002) 359-366
76. Koella J.C. An evolutionary view of the interactions between anopheline mosquitoes and malaria parasites. Microbes Infect. 1 (1999) 303-308
77. Krueger A., Fischer P., and Morales-Hojas R. Molecular phylogeny of the filaria genus Onchocerca with special emphasis on Afrotropical human and bovine parasites. Acta Trop. 101 (2007) 1-14
78. Laurence B.R. Intake and migration of the microfilariae of Onchocerca volvulus (Leuckart) in Simulium damnosum Theobald. J. Helminthol. 40 (1966) 337-342
79. Laurence B.R., and Pester F.R. Adaptation of a filarial worm, Brugia patei, to a new mosquito host, Aedes togoi. J. Helminthol. 41 (1967) 365-392
80. Lehane M.J. Peritrophic matrix structure and function. Annu. Rev. Entomol. 42 (1997) 525-550
81. Lewis D.J. A peritrophic membrane in Simulium. Nature 165 (1950) 978
82. Lewis D.J. Simulium damnosum and its relation to onchocerciasis in the Anglo-Egyptian Sudan. Bull. Entomol. Res. 43 (1953) 597-644
83. Lewis D.J., and Garnham P.C.C. The Simuliidae (Diptera) of British Honduras. Bull. Entomol. Res. 50 (1959) 703-710
84. Lively C.M. Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43 (1989) 1663-1671
85. Lively C.M., and Jokela J. Clinical variation for local adaptation in a host-parasite interaction. Proc. R. Soc. Lond. B 263 (1996) 891-897
86. Macdonald G. The Epidemiology and Control of Malaria (1957), Oxford University Press, London
87. Macdonald G. The dynamics of helminth infections, with special reference to schistosomes. Trans. R. Soc. Trop. Med. Hyg. 59 (1965) 489-506
88. Mackenzie C.D. Efficacy of ivermectin against Onchocerca volvulus in Ghana. Correspondence apropos Osei-Atweneboana et al. (2007). Lancet 370 (2007) 1123
89. Maia-Herzog M., Shelley A.J., Bradley J.E., Luna Dias A.P., Calvão R.H., Lowry C., Camargo M., Rubio J.M., Post R.J., and Coelho G.E. Discovery of a new focus of human onchocerciasis in central Brazil. Trans. R. Soc. Trop. Med. Hyg. 93 (1999) 235-239
90. May R.M. Togetherness among schistosomes: Its effects on the dynamics of the infection. Math. Biosci. 35 (1977) 301-343
91. May R.M., and Woolhouse M.E.J. Biased sex ratios and parasite mating probabilities. Parasitology 107 (1993) 287-295
92. McGreevy P.B., Bryan J.H., Oothuman P., and Kolstrup N. On the lethal effects of the cibarial and pharyngeal armatures of mosquitoes on microfilariae. Trans. R. Soc. Trop. Med. Hyg. 72 (1978) 361-368
93. Morales-Hojas R., Cheke R.A., and Post R.J. A preliminary analysis of the population genetics and molecular phylogenetics of Onchocerca volvulus (Nematoda: Filarioidea) using nuclear ribosomal second internal transcribed spacer sequences. Mem. Inst. Oswaldo Cruz 102 (2007) 879-882
94. Omar M.S., and Garms R. The fate and migration of microfilariae of a Guatemalan strain of Onchocerca volvulus in Simulium ochraceum and S. metallicum, and the role of the buccopharyngeal armature in the destruction of microfilariae. Tropenmed. Parasitol. 26 (1975) 183-190
95. Omar M.S., and Garms R. Lethal damage to Simulium metallicum following high intakes of Onchocerca volvulus microfilariae in Guatemala. Tropenmed. Parasitol. 28 (1977) 109-119
96. Omar M.S., Denke A.M., and Raybould J.N. The development of Onchocerca ochengi (Nematoda: Filarioidea) to the infective stage in Simulium damnosum s.l. with a note on the histochemical staining of the parasite. Tropenmed. Parasitol. 30 (1979) 157-162
97. Osei-Atweneboana M.Y., Eng J.K., Boakye D.A., Gyapong J.O., and Prichard R.K. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: A two-phase epidemiological study. Lancet 369 (2007) 2021 2019
98. Parker M.A. Local population differentiation for compatibility in an annual legume and its host-specific pathogen. Evolution 39 (1985) 713-723
99. Philippon B. Étude de la transmission d'Onchocerca volvulus (Leuckart, 1893) (Nematoda, Onchocercidae) par Simulium damnosum Theobald, 1903 (Diptera: Simuliidae) en Afrique tropicale. Travaux et Documents de l' O.R.S.T.O.M. (1977) (Paris) No. 63
100. Philippon B., and Bain O. Transmission de l'onchocercose humaine en zone de savane d'Afrique Occidentale, passage des microfilaires d'Onchocerca volvulus Leuck. dans l'hémocèle de la femelle de Simulium damnosum Th. Cahiers O.R.S.T.O.M. sér. Entomol. méd. Parasitol. 10 (1972) 251-261
101. Phiri J., and Ham P.J. Enhanced migration of Brugia pahangi microfilariae through the mosquito midgut following N acetyl D glucosamine ingestion. Trans. R. Soc. Trop. Med. Hyg. 84 (1990) 462
102. Pichon G. Relations mathematiques entre le nombre des microfilaires ingérées et le nombre des parasites chez différents vecteurs natureles ou expérimentaux de filarioses. Cahiers O.R.S.T.O.M. sér. Entomol. méd. Parasitol. 12 (1974) 199-216
103. Pichon G., Perrault G., and Laigret J. Rendement parasitaire chez les vecteurs de filarioses. Bull. World Health Organ. 51 (1974) 517-524
104. Post R.J., Mustapha M., and Krueger A. Taxonomy and inventory of the cytospecies and cytotypes of the Simulium damnosum complex (Diptera: Simuliidae) in relation to onchocerciasis. Trop. Med. Int. Health 12 (2007) 1342-1353
105. Poulin R. Evolution and phylogeny of behavioural manipulation of insect hosts by parasites. Parasitology 116 Suppl 1 (1998) S3-S11
106. Ramos A., Mahowald A., and Jacobs-Lorena M. Gut-specific genes from the black fly Simulium vittatum encoding trypsin-like and carboxypeptidase-like proteins. Insect Mol. Biol. 1 (1993) 149-163
107. Ramos A., Mahowald A., and Jacobs-Lorena M. Peritrophic matrix of the black fly Simulium vittatum: formation, structure, and analysis of its protein components. J. Exp. Zool. 268 (1994) 269-281
108. Reid G.D.F. Cibarial armature of Simulium vectors of onchocerciasis. Trans. R. Soc. Trop. Med. Hyg. 72 (1978) 438
109. Reid G.D.F. Structure and function of the cibarial armature in Simuliidae. Med. Vet. Entomol. 8 (1994) 295-301
110. Reid G.D.F., and Lehane M.J. Peritrophic membrane formation in three temperate simuliids, Simulium ornatum, S. equinum and S. lineatum, with respect to the migration of onchocercal microfilariae. Ann. Trop. Med. Parasitol. 78 (1984) 527-539
111. Remme J.H.F., Amazigo U., Engels D., Barryson A., and Yameogo L. Efficacy of ivermectin against Onchocerca volvulus in Ghana. Correspondence apropos Osei-Atweneboana et al. (2007). Lancet 370 (2007) 1123-1124
112. Renshaw M., and Hurd H. The effects of Onchocerca lienalis infection on vitellogenesis in the British blackfly Simulium ornatum. Parasitology 109 (1994) 337-343
113. Renshaw M., and Hurd H. Vitellogenin sequestration by Simulium oocytes: The effect of Onchocerca infection. Physiol. Entomol. 19 (1994) 70-74
114. 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. 81 (1987) 239-252
115. Renz A., and Wenk P. The distribution of the microfilariae of Onchocerca volvulus in the different body regions in relation to the attacking behaviour of Simulium damnosum s.l. in the Sudan savanna of northern Cameroon. Trans. R. Soc. Trop. Med. Hyg. 77 (1983) 748-752
116. Richards F.O., Boatin B., Sauerbrey M., and Sékétéli A. Control of onchocerciasis today: status and challenges. Trends Parasitol. 17 (2001) 558-563
117. Richardson D.M., and Pyek P. Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog. Phys. Geog. 30 (2006) 409-431
118. Rothfels K. Speciation in black flies. Genome 32 (1989) 500-509
119. Schiller E.L., Petersen J.L., Shirazian D., and Figueroa Marroquín H. Morphogenesis of larval Onchocerca volvulus in the Panamanian black fly, Simulium quadrivittatum. Am. J. Trop. Med. Hyg. 33 (1984) 410-413
120. Schulz Key H. Observations on the reproductive biology of Onchocerca volvulus. Acta Leiden. 59 (1990) 27-43
121. Schulz Key H., and Karam M. Periodic reproduction of Onchocerca volvulus. Parasitol. Today 2 (1986) 284-286
122. Schwab A.E., Churcher T.S., Schwab A.J., Basáñez M.G., and Prichard R.K. An analysis of the population genetics of potential multi-drug resistance in Wuchereria bancrofti due to combination chemotherapy. Parasitology 134 (2007) 1025-1040
123. Shao L., Devenport M., and Jacobs-Lorena M. The peritrophic matrix of hematophagous insects. Arch. Insect Biochem. Physiol. 47 (2001) 119-125
124. Shelley A.J. Vector aspects of the epidemiology of onchocerciasis in Latin America. Annu. Rev. Entomol. 30 (1988) 337-366
125. Shelley A.J. Simuliidae and the transmission and control of human onchocerciasis in Latin American. Cad Saúde Publica R. Janeiro 7 (1991) 310-327
126. Shelley A.J., and Arzube M. Studies on the biology of Simuliidae (Diptera) at the Santiago focus in Ecuador, with special reference to the vectors and disease transmission. Trans. R. Soc. Trop. Med. Hyg. 79 (1985) 328-338
127. Shelley A.J., Charalambous M., and Arzube M. Onchocerca volvulus development in four Simulium exiguum cytospecies in Ecuador. Bull. Soc. Fr. Parasitol. 8 (1990) 1145
128. Shelley A.J., Luna Dias A.P.A., Moraes M.A.P., and Procunier W.S. The status of Simulium oyapockense and S. limbatum as vectors of human onchocerciasis in Brazilian Amazonia. Med. Vet. Entomol. 1 (1987) 219-234
129. Shelley A.J., Procunier W.S., and Arzube M. Desarrollo de Onchocerca volvulus en dos citoespecies de Simulium exiguum complex (Diptera: Simuliidae) en el Ecuador. Rev. Ecuat. Hig. Med. Trop. 39 (1989) 9-23
130. Sinden R.E., Dawes E.J., Alavi Y., Waldock J., Finney O., Mendoza J., Butcher G.A., Andrews L., Hill A.V., Gilbert S.C., and Basáñez M.G. Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathog. 3 (2007) e195
131. Soumbey-Alley E., Basáñez M.G., Bissan Y., Boatin B.A., Remme J.H.F., Nagelkerke N.J.D., De Vlas S.J., Borsboom G.J.J.M., and Habbema J.D.F. Uptake of Onchocerca volvulus (Nematoda: Onchocercidae) by Simulium (Diptera: Simuliidae) is not strongly dependent on the density of skin microfilariae in the human host. J. Med. Entomol. 41 (2004) 83-94
132. Stallings T., Cupp M.S., and Cupp E.W. Orientation of Onchocerca lienalis Stiles (Filarioidea: Onchocercidae) microfilariae to black fly saliva. J. Med. Entomol. 39 (2002) 908-914
133. Subramanian S., Krishnamoorthy K., Ramaiah K.D., Habbema J.D.F., Das P.K., and Plaisier A.P. Relationship between microfilarial load in the human host and uptake and development of Wuchereria bancrofti microfilariae by Culex quinquefasciatus: a study under natural conditions. Parasitology 116 (1998) 243-255
134. Sutcliffe J.F. Anatomy of membranous mouthpart cuticles and their roles in feeding in black flies (Diptera: Simuliidae). J. Morphol. 186 (1985) 53-68
135. Sutcliffe J.F., and McIver S.B. Mechanics of blood-feeding in black flies (Diptera, Simuliidae). J. Morphol. 180 (1984) 125-144
136. Takaoka H., Tada I., Hashiguchi Y., Baba M., Korenaga M., Ochoa J.O., and Convit J. Experimental infections of three Guatemalan blackfly species with North Venezuelan Onchocerca volvulus. Jpn. J. Sanitary Zool. 37 (1986) 319-323
137. Takaoka H., Tada I., Hashiguchi Y., Baba M., Korenaga M., Ochoa J.O., Convit J., and Yarzábal L. A cross-compatibility study of Guatemalan and North Venezuelan Onchocerca volvulus to Simulium metallicum from two countries. Jpn. J. Parasitol. 35 (1986) 35-41
138. Tang J., Toé L., Back C., Zimmerman P.A., Pruess K., and Unnasch T.R. The Simulium damnosum species complex: Phylogenetic analysis and molecular identification based upon mitochondrially encoded gene sequences. Insect Mol. Biol. 4 (1995) 79-88
139. Tidwell M.A., Tidwell M.A., Muñoz De Hoyos P., and Corredor A. Simulium exiguum, the vector of Onchocerca volvulus on the Río Micay, Colombia. Am. J. Trop. Med. Hyg. 29 (1980) 377-381
140. Toé L., Tang J., Back C., Katholi C.R., and Unnasch T.R. Vector-parasite transmission complexes for onchocerciasis in West Africa. Lancet 349 (1997) 163-166
141. Vajime C.G., and Dunbar R.W. Chromosomal identification of eight species of the subgenus Edwardsellum near and including Simulium (Edwardsellum) damnosum Theobald (Diptera: Simuliidae). Tropenmed. Parasitol. 26 (1975) 111-138
142. Vieira J.C., Brackenboro L., Porter C.H., Basáñez M.G., and Collins R.C. Temporal and spatial variation in biting rates and parasite transmission potentials of onchocerciasis vectors in Ecuador. Trans. R. Soc. Trop. Med. Hyg. 99 (2005) 178-195
143. Vivas-Martínez S., Basáñez M.G., Grillet M.E., Weiss H., Botto C., García M., Villamizar N.J., and Chavasse D.C. Onchocerciasis in the Amazonian focus of southern Venezuela: Altitude and blackfly species composition as predictors of endemicity to select communities for ivermectin control programmes. Trans. R. Soc. Trop. Med. Hyg. 92 (1998) 613-620
144. Vuong P., Bain O., Cabaret J., Petit G., Prod'hon J., Ranque P., and Chabaud A.G. Forest and savanna onchocerciasis: Comparative morphometric histopathology of skin lesions. Trop. Med. Parasitol. 39 (1988) 105-110
145. Wahl G., Ekale D., and Schmitz A. Onchocerca ochengi: Assessment of the Simulium vectors in north Cameroon. Parasitology 116 (1998) 327-336
146. Webster J.P., Gower C.M., and Blair L. Do hosts and parasites coevolve? Empirical support from the Schistosoma system. Am. Nat. 164 Suppl 5 (2004) S33-S51
147. Wetten S., Collins R.C., Vieira J.C., Marshall C., Shelley A.J., and Basáñez M.G. Vector competence for Onchocerca volvulus in the Simulium (Notolepria) exiguum complex: Cytoforms or density-dependence?. Acta Trop. 103 (2007) 58-68
148. White M.J.D. Modes of Speciation (1978), W. H. Freeman and Co., San Francisco
149. Williams C.B. The use of logarithms in the interpretation of certain entomological problems. Ann. Appl. Biol. 24 (1937) 404-414
150. Woolhouse M.E.J., Webster J.P., Domingo E., Charlesworth B., and Levin B.R. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32 (2002) 569-577
151. Zimmerman P.A., Dadzie K.Y., De Sole G., Remme J., Soumbey Alley E., and Unnasch T.R. Onchocerca volvulus DNA classification correlates with epidemiological patterns of blindness. J. Infect. Dis. 165 (1992) 964-968
152. Zimmerman P.A., Katholi C.R., Wooten M.C., Lang-Unnasch N., and Unnasch T.R. Recent evolutionary history of American Onchocerca volvulus, based on analysis of a tandemly repeated DNA sequence family. Mol. Biol. Evol. 11 (1994) 384-392