Ivermectin to reduce malaria transmission: A research agenda for a promising new tool for elimination

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Chaccour, Carlos J ^a,b   Kobylinski, Kevin C ^c   Bassat, Quique ^d,e   Bousema, Teun ^f,g   Drakeley, Chris ^f   Alonso, Pedro ^d,e   Foy, Brian D ^h  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

^e Manhiça Health Research Center   (Mozambique)

^f LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^g RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^h Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Endectocides; Ivermectin; Malaria elimination; Vector control

Indexed keywords

ARTEMISININ; IVERMECTIN;

ANOPHELES; ARTICLE; BLURRED VISION; COLOR VISION; DISEASE ELIMINATION; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG SAFETY; DRUG TOLERABILITY; HUMAN; LYMPHATIC FILARIASIS; MALARIA; NEUROTOXICITY; NONHUMAN; ONCHOCERCIASIS; POPULATION DYNAMICS; SIDE EFFECT; SINGLE DRUG DOSE; VECTOR CONTROL;

ANIMALS; ANOPHELES; ANTIPARASITIC AGENTS; CLINICAL TRIALS AS TOPIC; HUMANS; INSECTICIDES; IVERMECTIN; MALARIA; MOSQUITO CONTROL;

EID: 84877044725     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-153     Document Type: Article

References (62)

1. A research agenda to underpin malaria eradication. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, Mendis K, Newman RD, Plowe CV, Rodriguez MH, Sinden R, Slutsker L, Tanner M, PLoS Med 2011 8 1000406 10.1371/journal.pmed.1000406 21311579
2. Malaria: progress, perils, and prospects for eradication. Greenwood BM, Fidock DA, Kyle DE, Kappe SH, Alonso PL, Collins FH, Duffy PE, J Clin Invest 2008 118 1266 1276 10.1172/JCI33996 18382739 (Pubitemid 351500419)
3. Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M, Malar J 2009 8 70 10.1186/1475-2875-8-70 19374767
4. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, Trends Parasitol 2011 27 91 98 10.1016/j.pt.2010.08.004 20843745
5. Artemisinin resistance in Plasmodium falciparum malaria. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NP, Lindegardh N, Socheat D, White NJ, N Engl J Med 2009 361 455 467 10.1056/NEJMoa0808859 19641202
6. Artemisinin resistance: current status and scenarios for containment. Dondorp AM, Yeung S, White L, Nguon C, Day NP, Socheat D, von Seidlein L, Nat Rev Microbiol 2010 8 272 280 20208550
7. Roll Back Malaria Partnership, The Global Malaria Action Plan Geneva 2008 http://www.rbm.who.int/gmap/gmap.pdf (accessed 28/04/2013)
8. The changing epidemiology of malaria elimination: new strategies for new challenges. Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG, Lancet 2013 in press
9. A research agenda for malaria eradication: vector control. The malERA Consultative Group on Vector Control, PLoS Med 2011 8 1000401 21311587
10. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Cote d'Ivoire. Edi CV, Koudou BG, Jones CM, Weetman D, Ranson H, Emerg Infect Dis 2012 18 1508 1511 10.3201/eid1809.120262 22932478
11. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Govella NJ, Ferguson H, Front Physiol 2012 3 199 22701435
12. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Kelly-Hope LA, McKenzie FE, Malar J 2009 8 19 10.1186/1475-2875-8-19 19166589
13. Ivermectin: 25 years and still going strong. Omura S, Int J Antimicrob Agents 2008 31 91 98 18037274
14. Ivermectin: uses and impact 20 years on. Fox LM, Curr Opin Infect Dis 2006 19 588 593 10.1097/QCO.0b013e328010774c 17075336 (Pubitemid 44665466)
15. Mectizan Donation Program, Annual Highlights 2011 http://www.mectizan. org/sites/www.mectizan.org/files/attachments/resources/ Annual%20Highlights%202011%20English.pdf (accessed 28/04/2013)
16. The effect of oral anthelmintics on the survivorship and re-feeding frequency of anthropophilic mosquito disease vectors. Kobylinski KC, Deus KM, Butters MP, Hongyu T, Gray M, da Silva IM, Sylla M, Foy BD, Acta Trop 2010 116 119 126 10.1016/j.actatropica.2010.06.001 20540931
17. Mortality and infertility in adult mosquitoes after the ingestion of blood containing ivermectin. Tesh RB, Guzman H, AmJTrop Med Hyg 1990 43 229 233 (Pubitemid 20348446)
18. Avermectins in arthropod vector management-prospects and pitfalls. Wilson ML, Parasitol Today 1993 9 83 87 10.1016/0169-4758(93)90210-7 15463716 (Pubitemid 23051179)
19. Effect of ivermectin on Anopheles gambiae mosquitoes fed on humans: the potential of oral insecticides in malaria control. Chaccour C, Lines J, Whitty CJ, J Infect Dis 2010 202 113 116 10.1086/653208 20482251
20. The potential of ivermectin to control the malaria vector Anopheles farauti. Foley DH, Bryan JH, Lawrence GW, Trans R Soc Trop Med Hyg 2000 94 625 628 10.1016/S0035-9203(00)90211-6 11198644
21. Mass treatment with ivermectin for filariasis control in Papua New Guinea: impact on mosquito survival. Bockarie MJ, Hii JL, Alexander ND, Bockarie F, Dagoro H, Kazura JW, Alpers MP, Med Vet Entomol 1999 13 120 123 10.1046/j.1365-2915.1999.00159.x 10484157 (Pubitemid 29405027)
22. Ivermectin mass drug administration to humans disrupts malaria parasite transmission in Senegalese villages. Kobylinski KC, Sylla M, Chapman PL, Sarr MD, Foy BD, AmJTrop Med Hyg 2011 85 3 5 10.4269/ajtmh.2011.11-0160
23. Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Sylla M, Kobylinski KC, Gray M, Chapman PL, Sarr MD, Rasgon JL, Foy BD, Malar J 2010 9 365 10.1186/1475-2875-9-365 21171970
24. Avermectins, MK-933 and MK-936, for mosquito control. Pampiglione S, Majori G, Petrangeli G, Romi R, Trans R Soc Trop Med Hyg 1985 79 797 799 10.1016/0035-9203(85)90121-X 3832491
25. Evaluation of the action of ivermectin on blood-sucking mosquitoes. Iakubovich V, Zakharova NF, Alekseev AN, Alekseev EA, Med Parazitol (Mosk) 1989 3 60 64 (Pubitemid 19172594)
26. Lethal effects of ivermectin on Anopheles quadrimaculatus. Jones JW, Meisch MV, Meek CL, Bivin WS, J Am Mosq Control Assoc 1992 8 278 280 1402865
27. Effects of ivermectin in canine blood on Anopheles quadrimaculatus, Aedes albopictus and Culex salinarius. Gardner K, Meisch MV, Meek CL, Biven WS, J Am Mosq Control Assoc 1993 9 400 402 8126472
28. Toxicity of bloodmeals from ivermectin-treated cattle to Anopheles gambiae s.l. Fritz ML, Siegert PY, Walker ED, Bayoh MN, Vulule JR, Miller JR, Ann Trop Med Parasitol 2009 103 539 547 10.1179/000349809X12459740922138 19695159
29. Comparative evaluation of systemic drugs for their effects against Anopheles gambiae. Butters MP, Kobylinski KC, Deus KM, da Silva IM, Gray M, Sylla M, Foy BD, Acta Trop 2012 121 34 43 10.1016/j.actatropica.2011.10.007 22019935
30. Lethal and sublethal effects of avermectin/milbemycin parasiticides on the African malaria vector, Anopheles arabiensis. Fritz ML, Walker ED, Miller JR, J Med Entomol 2012 49 326 331 10.1603/ME11098 22493850
31. Duration of the mosquitocidal effect of ivermectin. Hooghof J, Lindsay SW, Drakeley C, Churcher T, Verhave JP, Kocken C, Sauerwein RW, Bousema T, Bastiaens G vGG, MW Journal 2012 3 1 5
32. Ivermectin inhibits the sporogony of Plasmodium falciparum in Anopheles gambiae. Kobylinski KC, Foy BD, Richardson JH, Malar J 2012 11 381 10.1186/1475-2875-11-381 23171202
33. Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology. Garrett-Jones C, Shidrawi GR, Bull World Health Organ 1969 40 531 545 5306719
34. The analysis of equilibrium in malaria. Macdonald G, Trop Dis Bull 1952 49 813 829 12995455
35. Endectocides for malaria control. Foy BD, Kobylinski KC, da Silva IM, Rasgon JL, Sylla M, Trends Parasitol 2011 27 423 428 10.1016/j.pt.2011.05.007 21727027
36. Possible pathogenic pathways in the adverse clinical events seen following ivermectin administration to onchocerciasis patients. Mackenzie CD, Geary TG, Gerlach JA, Filaria J 2003 2 1 5 10.1186/1475-2883-2-5 14975062 (Pubitemid 38751366)
37. Ivermectin detection in serum of onchocerciasis patients: relationship to adverse reactions. Njoo FL, Beek WM, Keukens HJ, van Wilgenburg H, Oosting J, Stilma JS, Kijlstra A, AmJTrop Med Hyg 1995 52 94 97
38. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Gardon J, Gardon-Wendel N, Demanga N, Kamgno J, Chippaux JP, Boussinesq M, Lancet 1997 350 18 22 10.1016/S0140- 6736(96)11094-1 9217715 (Pubitemid 27279765)
39. Validation of the rapid assessment procedure for loiasis (RAPLOA) in the democratic republic of Congo. Wanji S, Akotshi DO, Mutro MN, Tepage F, Ukety TO, Diggle PJ, Remme JH, Parasit Vectors 2012 5 25 10.1186/1756-3305-5-25 22300872
40. Viability of adult Onchocerca volvulus after six 2-weekly doses of ivermectin. Duke BO, Pacque MC, Munoz B, Greene BM, Taylor HR, Bull World Health Organ 1991 69 163 168 1860146
41. The chemotherapy of onchocerciasis. XIX: The clinical and laboratory tolerance of high dose ivermectin. Awadzi K, Opoku NO, Addy ET, Quartey BT, Trop Med Parasitol 1995 46 131 137 8525285
42. Safety, tolerability, and pharmacokinetics of escalating high doses of ivermectin in healthy adult subjects. Guzzo CA, Furtek CI, Porras AG, Chen C, Tipping R, Clineschmidt CM, Sciberras DG, Hsieh JY, Lasseter KC, J Clin Pharmacol 2002 42 1122 1133 10.1177/009127002401382731 12362927
43. Adverse systemic reactions to treatment of onchocerciasis with ivermectin at normal and high doses given annually or three-monthly. Kamgno J, Gardon J, Gardon-Wendel N, Demanga N, Duke BO, Boussinesq M, Trans R Soc Trop Med Hyg 2004 98 496 504 10.1016/j.trstmh.2003.10.018 15186939 (Pubitemid 38950379)
44. Merck & Co, Stromectrol. Package insert 2009 http://www.accessdata. fda.gov/drugsatfda-docs/label/2009/050742s026lbl.pdf (Accessed 28/04/2013)
45. Pregnancy outcome after inadvertent ivermectin treatment during community-based distribution. Pacque M, Munoz B, Poetschke G, Foose J, Greene BM, Taylor HR, Lancet 1990 336 1486 1489 10.1016/0140-6736(90)93187-T 1979100
46. Absence of any adverse effect of inadvertent ivermectin treatment during pregnancy. Chippaux JP, Gardon-Wendel N, Gardon J, Ernould JC, Trans R Soc Trop Med Hyg 1993 87 318 10.1016/0035-9203(93)90146-H 8236406
47. Ivermectin and pregnancy in mass treatment in Mali. Doumbo O, Soula G, Kodio B, Perrenoud M, Bull Soc Pathol Exot 1992 85 247 251 1422278
48. Inadvertent exposure of pregnant women to ivermectin and albendazole during mass drug administration for lymphatic filariasis. Gyapong JO, Chinbuah MA, Gyapong M, Trop Med Int Health 2003 8 1093 1101 10.1046/j.1360-2276.2003. 01142.x 14641844 (Pubitemid 38005410)
49. Efficacy of ivermectin and albendazole alone and in combination for treatment of soil-transmitted helminths in pregnancy and adverse events: a randomized open label controlled intervention trial in Masindi district, western Uganda. Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P, AmJTrop Med Hyg 2008 79 856 863
50. Changes in the use profile of Mectizan: 1987-1997. Brown KR, Ann Trop Med Parasitol 1998 92 Suppl 1 61 64 9861268
51. Ivermectin levels in human breastmilk. Ogbuokiri JE, Ozumba BC, Okonkwo PO, Eur J Clin Pharmacol 1993 45 389 390 8299677 (Pubitemid 23338553)
52. Effects of annual mass treatment with ivermectin for onchocerciasis on the prevalence of intestinal helminths. Gutman J, Emukah E, Okpala N, Okoro C, Obasi A, Miri ES, Richards FO Jr, AmJTrop Med Hyg 2010 83 534 541 10.4269/ajtmh.2010.10-0033
53. Moderate effect of artemisinin-based combination therapy on transmission of Plasmodium falciparum. Bousema JT, Schneider P, Gouagna LC, Drakeley CJ, Tostmann A, Houben R, Githure JI, Ord R, Sutherland CJ, Omar SA, Sauerwein RW, J Infect Dis 2006 193 1151 1159 10.1086/503051 16544256
54. Reduction of malaria transmission to Anopheles mosquitoes with a six-dose regimen of co-artemether. Sutherland CJ, Ord R, Dunyo S, Jawara M, Drakeley CJ, Alexander N, Coleman R, Pinder M, Walraven G, Targett GA, PLoS Med 2005 2 92 10.1371/journal.pmed.0020092 15839740 (Pubitemid 40721079)
55. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. Okell LC, Griffin JT, Kleinschmidt I, Hollingsworth TD, Churcher TS, White MJ, Bousema T, Drakeley CJ, Ghani AC, PLoS One 2011 6 20179 10.1371/journal.pone.0020179 21629651
56. Mass administrations of antimalarial drugs. von Seidlein L, Greenwood BM, Trends Parasitol 2003 19 452 460 10.1016/j.pt.2003.08.003 14519583 (Pubitemid 38366142)
57. A research agenda for malaria eradication: drugs. The malERA Consultative Group on Drugs, PLoS Med 2011 8 1000402 21311580
58. Consideration of ethics in primaquine therapy against malaria transmission. Baird JK, Surjadjaja C, Trends Parasitol 2011 27 11 16 10.1016/j.pt.2010.08.005 20846906
59. Human antibody response to Anopheles saliva for comparing the efficacy of three malaria vector control methods in Balombo. Brosseau L, Drame PM, Besnard P, Toto JC, Foumane V, Le Mire J, Mouchet F, Remoue F, Allan R, Fortes F, Carnevale P, Manguin S, Angola. PLoS One 2012 7 44189 10.1371/journal.pone. 0044189
60. IgG responses to Anopheles gambiae salivary antigen gSG6 detect variation in exposure to malaria vectors and disease risk. Stone W, Bousema T, Jones S, Gesase S, Hashim R, Gosling R, Carneiro I, Chandramohan D, Theander T, Ronca R, Modiano D, Arca B, Drakeley C, PLoS One 2012 7 40170 10.1371/journal.pone. 0040170 22768250
61. Novel vectors of malaria parasites in the western highlands of Kenya. Stevenson J, St Laurent B, Lobo NF, Cooke MK, Kahindi SC, Oriango RM, Harbach RE, Cox J, Drakeley C, Emerg Infect Dis 2012 18 1547 1549 10.3201/eid1809.120283 22932762
62. Phenotypic evidence of emerging ivermectin resistance in Onchocerca volvulus. Osei-Atweneboana MY, Awadzi K, Attah SK, Boakye DA, Gyapong JO, Prichard RK, PLoS Negl Trop Dis 2011 5 998 10.1371/journal.pntd.0000998 21468315