Administration of ivermectin to peridomestic cattle: A promising approach to target the residual transmission of human malaria

Malaria Journal

Volumn 14, Issue 1, 2015, Pages

  Pooda, Hermann S ^a,b,e   Rayaisse, Jean Baptiste ^a   Hien, Domonbabele François De Sale ^c   Lefèvre, Thierry ^c,d   Yerbanga, Serge R ^c   Bengaly, Zakaria ^a   Dabiré, Roch K ^c   Belem, Adrien M G ^e   Sidibé, Issa ^a,b   Solano, Philippe ^f   Mouline, Karine ^c,d  

^a Centre International de Recherche   (Burkina Faso)

^b Campagne Panafricaine d'Éradication de la Mouche Tsé tsé et des Trynaposomoses   (Burkina Faso)

^c Direction Régionale de l'Ouest de l'Institut de Recherche en Sciences de la Santé   (Burkina Faso)

^d UNIV MONTPELLIER   (France)

^e Polytechnic University of Bobo Dioulasso   (Burkina Faso)

^f Institut de recherche pour le développement   (France)

Author keywords

Anopheles coluzzii; Cattle; Fecundity; Infectivity; Ivermectin; Malaria; One Health; Survival; West Africa

Indexed keywords

IVERMECTIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOPHELES; ANOPHELES COLUZZII; ARTICLE; BOVINE; BULL (BOVINE); BURKINABE CATTLE; CALF (BOVINE); CONCENTRATION RESPONSE; CONTROLLED STUDY; EGG PRODUCTION; FEMALE; FERTILITY; GENE MUTATION; HOST PARASITE INTERACTION; INFECTION SENSITIVITY; INSECTICIDAL ACTIVITY; KDR GENE; MALARIA; MALE; MORTALITY; NONHUMAN; PARASITE TRANSMISSION; SURVIVAL RATE; VECTOR CONTROL; ZOONOSIS;

EID: 84951030889     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-1001-z     Document Type: Article

References (55)

1. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control. Trends Parasitol. 2011;27:91-8.
2. Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med Vet Entomol. 2012;26:103-5.
3. Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.
4. Killeen GF. Characterizing, controlling and eliminating residual malaria transmission. Malar J. 2014;13:330.
5. Chaccour C, Kobylinsky K, Bassat Q, Boussema T, Drakeley C, Alonso P, et al. Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013;12:153.
6. Chaccour CJ, Rabinovich NR, Slater H, Canavati SE, Bousema T, Lacerda M, ter Kuile F, Drakeley C, Bassat Q, Foy BD, Kobylinski K. Establishment of the Ivermectin Research for Malaria Elimination Network: updating the research agenda. Malar J. 2015;14:243.
7. Shoope WL, Soll MD. Chemistry, pharmacology and safety of the macrocyclic lactones. In: Wercruysse J, Rew RS, editors. Macrocyclic lactones in antiparasitic therapy. CAB Intern; 2002. p. 1-29.
8. Amazigo U. The African Programme for Onchocerciasis Control (APOC). Ann Trop Med Parasitol. 2008;102(Suppl 1):19-22.
9. Ottesen EA, Hooper PJ, Bradley M, Biswas G. The global programme to eliminate lymphatic filariasis: health impact after 8 years. PLoS Negl Trop Dis. 2008;2:e317.
10. Kobylinski KC, Deus KM, Butters MP, Hongyu T, Gray M, Da Silva IM, et al. The effect of oral anthelmintics on the survivorship and re-feeding frequency of anthropophilic mosquito disease vectors. Acta Trop. 2010;116:119-26.
11. Kobylinski KC, Sylla M, Chapman PL, Sarr MD, Foy BD. Ivermectin mass drug administration to humans disrupts malaria parasite transmission in Senegalese villages. Am J Trop Med Hyg. 2011;85:3-5.
12. Sylla M, Kobylinski KC, Gray M, Chapman PL, Sarr MD, Rasgon JL, et al. Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Malar J. 2010;9:365.
13. Foy BD, Kobylinski DKC, Da Silva IM, Rasgon JL, Sylla M. Endectocides for malaria control. Trends Parasitol. 2011;27:423-8.
14. Alout H, Krajacich BJ, Meyers JI, Grubaugh ND, Brackney DE, Kobylinski KC, et al. Evaluation of ivermectin mass drug administration for malaria transmission control across different West African environments. Malar J. 2014;13:417.
15. Ouedraogo A, Bastiaens G, Tiono A, Guelbeogo W, Kobylinski K, Ouedraogo A, et al. Efficacy and safety of the mosquitocidal drug ivermectin to prevent malaria transmission after treatment: a double-blind, randomized, clinical trial. Clin Infect Dis. 2015;60:357-65.
16. Kobylinski KC, Foy BD, Richardson JH. Ivermectin inhibits the sporogony of Plasmodium falciparum in Anopheles gambiae. Malar J. 2012;11:381.
17. Meyers JI, Gray M, Kuklinski W, Johnson LB, Snow CD, Black WC, et al. Characterization of the target of ivermectin, the glutamate-gated chloride channel, from Anopheles gambiae. J Exp Biol. 2015;218:1478-86.
18. Cully DF, Vassilatis DK, Liu KK, Paress PS, Van der Ploeg LHT, Schaeffer JM, et al. Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature. 1994;371:707-11.
19. Cully DF, Paress PS, Liu KK, Schaeffer JM, Arena JP. Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. J Biol Chem. 1996;271:20187-91.
20. Ndiath MO, Mazenot C, Sokhna C, Trape JF. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLoS One. 2014;9:e97700.
21. Lefèvre T, Gouagna LC, Dabiré KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81:1023-9.
22. Geary TG. Ivermectin 20 years on: maturation of a wonder drug. Trends Parasitol. 2005;21:1985-7.
23. Pooda SH, Mouline K, De Meeûs T, Bengaly Z, Solano P. Decrease in survival and fecundity of Glossina palpalis gambiensis vanderplank 1949 (Diptera: Glossinidae) fed on cattle treated with single doses of ivermectin. Parasites. 2013;6:1-6.
24. INSD. Recensement general de la population et de l'habitation de 2006 Juillet 2008; 2008.
25. Naz S, Maqbool A, Ahmad M-D, Anjum AA, Zaman S. Efficacy of ivermectin for control of zoophilic malaria vectors in Pakistan. Pak J Zool. 2013;45:1585-91.
26. Poché RM, Burruss D, Polyakova L, Poché DM, Garlapati RB. Treatment of livestock with systemic insecticides for control of Anopheles arabiensis in western Kenya. Malar J. 2015;14:351.
27. Fritz ML, Siegert PY, Walker ED, Bayoh MNI, Vulule JRI. Toxicity of bloodmeals from ivermectin-treated cattle to Anopheles gambiae s.l. Ann Trop Med Parasitol. 2009;103:539-47.
28. Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, della Torre A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J. 2008;7:163.
29. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179-84.
30. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, et al. Comparative genomics: insecticide resistance in mosquito vectors. Nature. 2003;423:136-7.
31. Namountougou M, Diabate A, Etang J, Bass C, Sawadogo SP, Gnankinie O, et al. First report of the L1014S kdr mutation in wild populations of Anopheles gambiae M and S molecular forms in Burkina Faso (West Africa). Acta Trop. 2013;125:123-7.
32. Hennesy D, Alvinerie M. Pharmacokinetics of macrocyclic lactones: conventional wisdom and news paradigms. In: Vercruysse J, Rew R, editors. Macrocyclic lactones in antiparasitic therapy. New York: CAB; 2002. p. 97-121.
33. Fernandes L, Briegel H. Reproductive physiology of Anopheles gambiae and Anopheles atroparvus. J Vector Ecol. 2005;30:11-26.
34. Mouline K, Mamai W, Agnew P, Tchonfienet M, Brengues C, Dabire R, et al. Physiology and development of the M and S molecular forms of Anopheles gambiae in Burkina Faso (West Africa). Med Vet Entomol. 2012;26:447-54.
35. Sangare I, Michalakis Y, Yameogo B, Dabire R, Morlais I, Cohuet A. Studying fitness cost of Plasmodium falciparum infection in malaria vectors: validation of an appropriate negative control. Malar J. 2013;12:2.
36. Alout H, Ndam TN, Sandeu MM, Djegbe I, Chandre F, Dabire RK, Djogbenou LS, Corbel V, Cohuet A. Insecticide resistance alleles affect vector competence of Anopheles gambiae s.s. for Plasmodium falciparum field isolates. PLoS One. 2013;8:e63849.
37. Vantaux A, Dabire KR, Cohuet A, Lefevre T. A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance. Malar J. 2014;13:442.
38. Crawley M. The R book, vol. 103. Silwood Park: Imperial College London; 2007.
39. Carnevale P, Robert V. Les Anophèles: Biologie. Marseille: Transmission Du Plasmodium et Lutte Antivectorielle. IRD; 2009.
40. Abbott WS. A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc. 1987;3:302-3.
41. Derua YA, Kisinza WN, Simonsen PE. Differential effect of human ivermectin treatment on blood feeding Anopheles gambiae and Culex quinquefasciatus. Parasit Vectors. 2015;8:130.
42. Lanusse C, Lifschitz A, Virkel G, Alvarez L, Sanchez S, Sutra JF, et al. Comparative plasma disposition kinetics of ivermectin, moxidectin and doramectin in cattle. J Vet Pharmacol Ther. 1997;20:91-9.
43. Alvinerie M, Escudero E, Sutra JF, Eeckhoutte C, Galtier P. The pharmacokinetics of moxidectin after oral and subcutaneous administration to sheep. Vet Res. 1998;29:113-8.
44. Tesh RB, Guzman H. Mortality and infertility in adult mosquitoes after the ingestion of blood containing ivermectin. Am J Trop Med Hyg. 1990;43:229-33.
45. Scott TW, Githeko AK, Fleisher A, Harrington LC, Yan G. DNA profiling of human blood in anophelines from lowland and highland sites in western Kenya. Am J Trop Med Hyg. 2006;75:231-7.
46. Deus KM, Saavedra-Rodriguez K, Butters MP, Black WC, Foy BD. The effect of ivermectin in seven stains of Aedes aegypti (Diptera: Culicidae) including a genetically diverse laboratory strain and three permethrin resistant strains. J Med Entomol. 2012;49:356-63.
47. Namountougou M, Simard F, Baldet T, Diabate A, Ouedraogo JB, Martin T, et al. Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS One. 2012;9:e48412.
48. Jones CM, Toe HK, Sanou A, Namountougou M, Hughes A, Diabate A, et al. Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS One. 2012;7:e45995.
49. Geurden T, Chartier C, Fanke J, di Regalbono AF, Traversa D, von Samson-Himmelstjerna G, et al. Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. Int J Parasitol Drugs Drug Resist. 2015;5:163-71.
50. Seaman J, Alout H, Meyers JI, Stenglein MD, Dabiré RK, Lozano-Fuentes S, et al. Age and prior blood feeding of Anopheles gambiae influences their susceptibility and gene expression patterns to ivermectin-containing blood meals. BMC Genom. 2015;16:797.
51. Lumaret J-P, Errouissi F. Use of anthelmintics in herbivores and evaluation of risks for the non target fauna of pastures. Vet Res. 2002;33:547-62.
52. Verdú JR, Cortez V, Ortiz AJ, González-Rodríguez E, Martinez-Pinna J, Lumaret J-P, et al. Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Sci Rep. 2015;5:13912.
53. Puniamoorthy N, Schäfer MA, Römbke J, Meier R, Blanckenhorn WU. Ivermectin sensitivity is an ancient trait affecting all ecdysozoa but shows phylogenetic clustering among sepsid flies. Evol Appl. 2014;7:548-54.
54. Slater HC, Walker PG, Bousema T, Okell LC, Ghani AC. The potential impact of adding ivermectin to a mass treatment intervention to reduce malaria transmission: a modelling study. J Infect Dis. 2014;210:1972-80.
55. Chaccour C, Barrio ÁI, Royo AGG, Urbistondo DM, Slater H, Hammann F, Del Pozo JL. Screening for an ivermectin slow-release formulation suitable for malaria vector control. Malar J. 2015;14:102.