Skip to main content
Top
Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Evaluation of ivermectin mass drug administration for malaria transmission control across different West African environments

Authors: Haoues Alout, Benjamin J Krajacich, Jacob I Meyers, Nathan D Grubaugh, Doug E Brackney, Kevin C Kobylinski, Joseph W Diclaro II, Fatorma K Bolay, Lawrence S Fakoli, Abdoulaye Diabaté, Roch K Dabiré, Roland W Bougma, Brian D Foy

Published in: Malaria Journal | Issue 1/2014

Login to get access

Abstract

Background

Mass drug administration (MDA) of ivermectin to humans for control and elimination of filarial parasites can kill biting malaria vectors and lead to Plasmodium transmission reduction. This study examines the degree and duration of mosquitocidal effects resulting from single MDAs conducted in three different West African countries, and the subsequent reductions in parity and Plasmodium sporozoite rates.

Methods

Indoor-resting, blood-fed and outdoor host-seeking Anopheles spp. were captured on days surrounding MDAs from 2008–2013 in Senegalese, Liberian and Burkinabé villages. Mortality was assessed on a portion of the indoor collection, and parity status was determined on host-seeking mosquitoes. The effect of MDA was then analysed against the time relative to the MDA, the distributed drugs and environmental variables.

Results

Anopheles gambiae survivorship was reduced by 33.9% for one week following MDA and parity rates were significantly reduced for more than two weeks after the MDAs. Sporozoite rates were significantly reduced by >77% for two weeks following the MDAs in treatment villages despite occurring in the middle of intense transmission seasons. These observed effects were consistent across three different West African transmission dynamics.

Conclusions

These data provide a comprehensive and crucial evidence base for the significant reduction in malaria transmission following single ivermectin MDAs across diverse field sites. Despite the limited duration of transmission reduction, these results support the hypothesis that repeated MDAs with optimal timing could help sustainably control malaria as well as filarial transmission.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO: World Malaria Report. 2013, Geneva: World Health Organization WHO: World Malaria Report. 2013, Geneva: World Health Organization
2.
go back to reference Pluess B, Tanser FC, Lengeler C, Sharp BL: Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010, 4: CD006657-PubMed Pluess B, Tanser FC, Lengeler C, Sharp BL: Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010, 4: CD006657-PubMed
3.
go back to reference 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: 91-98. 10.1016/j.pt.2010.08.004.CrossRefPubMed 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: 91-98. 10.1016/j.pt.2010.08.004.CrossRefPubMed
4.
go back to reference Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C: Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet. 2011, 11: 925-932. 10.1016/S1473-3099(11)70194-3.CrossRefPubMed Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C: Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet. 2011, 11: 925-932. 10.1016/S1473-3099(11)70194-3.CrossRefPubMed
5.
go back to reference Mita T, Tanabe K: Evolution of Plasmodium falciparum drug resistance: implications for the development and containment of artemisinin resistance. Jpn J Infect Dis. 2012, 65: 465-475. 10.7883/yoken.65.465.CrossRefPubMed Mita T, Tanabe K: Evolution of Plasmodium falciparum drug resistance: implications for the development and containment of artemisinin resistance. Jpn J Infect Dis. 2012, 65: 465-475. 10.7883/yoken.65.465.CrossRefPubMed
6.
go back to reference The malERA Consultative Group on Vector Control: A research agenda for malaria eradication: vector control. PLoS Med. 2011, 8: e1000401-PubMedCentralCrossRef The malERA Consultative Group on Vector Control: A research agenda for malaria eradication: vector control. PLoS Med. 2011, 8: e1000401-PubMedCentralCrossRef
7.
go back to reference Mectizan Donation Program: Mectizan Annual Highligths. 2013 Mectizan Donation Program: Mectizan Annual Highligths. 2013
8.
go back to reference Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, Foy BD: Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013, 12: 153-10.1186/1475-2875-12-153.PubMedCentralCrossRefPubMed Chaccour CJ, Kobylinski KC, Bassat Q, Bousema T, Drakeley C, Alonso P, Foy BD: Ivermectin to reduce malaria transmission: a research agenda for a promising new tool for elimination. Malar J. 2013, 12: 153-10.1186/1475-2875-12-153.PubMedCentralCrossRefPubMed
9.
go back to reference Bockarie MJ, Hii JL, Alexander N, Bockarie F, Dagoro H, Kazura JW, Alpers MP: Mass treatment with ivermectin for filariasis control in Papua New Guinea: impact on mosquito survival. Med Vet Entomol. 1999, 13: 120-123. 10.1046/j.1365-2915.1999.00159.x.CrossRefPubMed Bockarie MJ, Hii JL, Alexander N, Bockarie F, Dagoro H, Kazura JW, Alpers MP: Mass treatment with ivermectin for filariasis control in Papua New Guinea: impact on mosquito survival. Med Vet Entomol. 1999, 13: 120-123. 10.1046/j.1365-2915.1999.00159.x.CrossRefPubMed
10.
go back to reference Sylla M, Kobylinski KC, Gray M, Chapman PL, Sarr MD, Rasgon JL, Foy BD: Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Malar J. 2010, 9: 365-10.1186/1475-2875-9-365.PubMedCentralCrossRefPubMed Sylla M, Kobylinski KC, Gray M, Chapman PL, Sarr MD, Rasgon JL, Foy BD: Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Malar J. 2010, 9: 365-10.1186/1475-2875-9-365.PubMedCentralCrossRefPubMed
11.
go back to reference Foy BD, Kobylinski KC, da Silva IM, Rasgon JL, Sylla M: Endectocides for malaria control. Trends Parasitol. 2011, 27: 423-428. 10.1016/j.pt.2011.05.007.PubMedCentralCrossRefPubMed Foy BD, Kobylinski KC, da Silva IM, Rasgon JL, Sylla M: Endectocides for malaria control. Trends Parasitol. 2011, 27: 423-428. 10.1016/j.pt.2011.05.007.PubMedCentralCrossRefPubMed
12.
go back to reference 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. 10.4269/ajtmh.2011.11-0160.PubMedCentralCrossRefPubMed 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. 10.4269/ajtmh.2011.11-0160.PubMedCentralCrossRefPubMed
13.
go back to reference Gething PW, Patil AP, Smith DL, Guerra C a, Elyazar IRF, Johnston GL, Tatem AJ, Hay SI: A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011, 10: 378-10.1186/1475-2875-10-378.PubMedCentralCrossRefPubMed Gething PW, Patil AP, Smith DL, Guerra C a, Elyazar IRF, Johnston GL, Tatem AJ, Hay SI: A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011, 10: 378-10.1186/1475-2875-10-378.PubMedCentralCrossRefPubMed
14.
go back to reference Krajacich BJ, Slade JR, Mulligan RF, LaBrecque B, Alout H, Grubaugh ND, Meyers JI, Fakoli LS, Bolay FK, Brackney DE, Burton TA, Seaman JA, Sylla M, Diclaro JW, Dabiré RK, Foy BD: Sampling host-seeking anthropophilic mosquito vectors in West Africa: comparisons of an active human-baited tent-trap against gold standard methods. Am J Trop Med Hyg. In press Krajacich BJ, Slade JR, Mulligan RF, LaBrecque B, Alout H, Grubaugh ND, Meyers JI, Fakoli LS, Bolay FK, Brackney DE, Burton TA, Seaman JA, Sylla M, Diclaro JW, Dabiré RK, Foy BD: Sampling host-seeking anthropophilic mosquito vectors in West Africa: comparisons of an active human-baited tent-trap against gold standard methods. Am J Trop Med Hyg. In press
15.
go back to reference Detinova TS: Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr Ser World Health Organ. 1962, 47: 13-191.PubMed Detinova TS: Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. Monogr Ser World Health Organ. 1962, 47: 13-191.PubMed
16.
go back to reference Fanello C, Santolamazza F, della Torre A: Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 2002, 16: 461-464. 10.1046/j.1365-2915.2002.00393.x.CrossRefPubMed Fanello C, Santolamazza F, della Torre A: Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 2002, 16: 461-464. 10.1046/j.1365-2915.2002.00393.x.CrossRefPubMed
17.
go back to reference Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Williamson MS, Field LM: PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008, 7: 177-10.1186/1475-2875-7-177.PubMedCentralCrossRefPubMed Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Williamson MS, Field LM: PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008, 7: 177-10.1186/1475-2875-7-177.PubMedCentralCrossRefPubMed
18.
go back to reference Kobylinski KC, Deus KM, Butters MP, Hongyu T, Gray M, da Silva IM, Sylla M, Foy BD: The effect of oral anthelmintics on the survivorship and re-feeding frequency of anthropophilic mosquito disease vectors. Acta Trop. 2010, 116: 119-126. 10.1016/j.actatropica.2010.06.001.PubMedCentralCrossRefPubMed Kobylinski KC, Deus KM, Butters MP, Hongyu T, Gray M, da Silva IM, Sylla M, Foy BD: The effect of oral anthelmintics on the survivorship and re-feeding frequency of anthropophilic mosquito disease vectors. Acta Trop. 2010, 116: 119-126. 10.1016/j.actatropica.2010.06.001.PubMedCentralCrossRefPubMed
19.
go back to reference Koella JC: On the use of mathematical models of malaria transmission. Acta Trop. 1991, 49: 1-25. 10.1016/0001-706X(91)90026-G.CrossRefPubMed Koella JC: On the use of mathematical models of malaria transmission. Acta Trop. 1991, 49: 1-25. 10.1016/0001-706X(91)90026-G.CrossRefPubMed
20.
go back to reference Slater HC, Walker PGT, 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, jiu351- Slater HC, Walker PGT, 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, jiu351-
21.
go back to reference Awadzi K, Edwards G, Duke BOL, Opoku NO, Attah SK, Addy ET, Ardrey AE, Quartey BT: The co-administration of ivermectin and albendazole: safety, pharmacokinetics and efficacy against Onchocerca volvulus. Ann Trop Med Parasitol. 2003, 97: 165-178. 10.1179/000349803235001697.CrossRefPubMed Awadzi K, Edwards G, Duke BOL, Opoku NO, Attah SK, Addy ET, Ardrey AE, Quartey BT: The co-administration of ivermectin and albendazole: safety, pharmacokinetics and efficacy against Onchocerca volvulus. Ann Trop Med Parasitol. 2003, 97: 165-178. 10.1179/000349803235001697.CrossRefPubMed
22.
go back to reference Garrett-Jones C: The assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the proportion of parous females. Bull World Health Organ. 1964, 31: 71-86.PubMedCentralPubMed Garrett-Jones C: The assessment of insecticidal impact on the malaria mosquito’s vectorial capacity, from data on the proportion of parous females. Bull World Health Organ. 1964, 31: 71-86.PubMedCentralPubMed
23.
go back to reference Rajatileka S, Burhani J, Ranson H: Mosquito age and susceptibility to insecticides. Trans R Soc Trop Med Hyg. 2011, 105: 247-253. 10.1016/j.trstmh.2011.01.009.CrossRefPubMed Rajatileka S, Burhani J, Ranson H: Mosquito age and susceptibility to insecticides. Trans R Soc Trop Med Hyg. 2011, 105: 247-253. 10.1016/j.trstmh.2011.01.009.CrossRefPubMed
24.
go back to reference Kobylinski KC, Foy BD, Richardson JH: Ivermectin inhibits the sporogony of Plasmodium falciparum in Anopheles gambiae. Malar J. 2012, 11: 381-10.1186/1475-2875-11-381.PubMedCentralCrossRefPubMed Kobylinski KC, Foy BD, Richardson JH: Ivermectin inhibits the sporogony of Plasmodium falciparum in Anopheles gambiae. Malar J. 2012, 11: 381-10.1186/1475-2875-11-381.PubMedCentralCrossRefPubMed
25.
go back to reference 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: 539-547. 10.1179/000349809X12459740922138.CrossRefPubMed 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: 539-547. 10.1179/000349809X12459740922138.CrossRefPubMed
26.
go back to reference Kamgno J, Gardon J, Gardon-Wendel N, Demanga-Ngangue , Duke BOL, Boussinesq M: Adverse systemic reactions to treatment of onchocerciasis with ivermectin at normal and high doses given annually or three-monthly. Trans R Soc Trop Med Hyg. 2004, 98: 496-504. 10.1016/j.trstmh.2003.10.018.CrossRefPubMed Kamgno J, Gardon J, Gardon-Wendel N, Demanga-Ngangue , Duke BOL, Boussinesq M: Adverse systemic reactions to treatment of onchocerciasis with ivermectin at normal and high doses given annually or three-monthly. Trans R Soc Trop Med Hyg. 2004, 98: 496-504. 10.1016/j.trstmh.2003.10.018.CrossRefPubMed
27.
go back to reference Heukelbach J, Winter B, Wikcke T, Muehlen M, Albrecht S, de Oliveira FA S, Sansigolo Kerr-Pontes LR, Liesenfeld O, Feldmeier H: Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull World Health Organ. 2004, 82: 563-571.PubMedCentralPubMed Heukelbach J, Winter B, Wikcke T, Muehlen M, Albrecht S, de Oliveira FA S, Sansigolo Kerr-Pontes LR, Liesenfeld O, Feldmeier H: Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull World Health Organ. 2004, 82: 563-571.PubMedCentralPubMed
28.
go back to reference Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, Kiniboro B, Zimmerman PA, Speed TP, Siba P, Felger I: Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A. 2012, 109: 10030-10035. 10.1073/pnas.1200841109.PubMedCentralCrossRefPubMed Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, Kiniboro B, Zimmerman PA, Speed TP, Siba P, Felger I: Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A. 2012, 109: 10030-10035. 10.1073/pnas.1200841109.PubMedCentralCrossRefPubMed
29.
go back to reference Kobylinski K, Alout H, Foy BD, Clements A, Adisakwattana P, Swierczewski B, Richardson J: Rationale for the co-administration of albendazole and ivermectin to humans for malaria parasite transmission control. Am J Trop Med Hyg. 2014, 91: 655-662. 10.4269/ajtmh.14-0187.PubMedCentralCrossRefPubMed Kobylinski K, Alout H, Foy BD, Clements A, Adisakwattana P, Swierczewski B, Richardson J: Rationale for the co-administration of albendazole and ivermectin to humans for malaria parasite transmission control. Am J Trop Med Hyg. 2014, 91: 655-662. 10.4269/ajtmh.14-0187.PubMedCentralCrossRefPubMed
30.
go back to reference Remme J, The CDI study group: Community-directed interventions for priority health problems in Africa: results of a multicountry study. Bull World Health Organ. 2010, 88: 509-518. 10.2471/BLT.09.069203.CrossRef Remme J, The CDI study group: Community-directed interventions for priority health problems in Africa: results of a multicountry study. Bull World Health Organ. 2010, 88: 509-518. 10.2471/BLT.09.069203.CrossRef
31.
go back to reference Blackburn BG, Eigege A, Gotau H, Gerlong G, Miri E, Hawley W a, Mathieu E, Richards F: Successful integration of insecticide-treated bed net distribution with mass drug administration in Central Nigeria. Am J Trop Med Hyg. 2006, 75: 650-655.PubMed Blackburn BG, Eigege A, Gotau H, Gerlong G, Miri E, Hawley W a, Mathieu E, Richards F: Successful integration of insecticide-treated bed net distribution with mass drug administration in Central Nigeria. Am J Trop Med Hyg. 2006, 75: 650-655.PubMed
Metadata
Title
Evaluation of ivermectin mass drug administration for malaria transmission control across different West African environments
Authors
Haoues Alout
Benjamin J Krajacich
Jacob I Meyers
Nathan D Grubaugh
Doug E Brackney
Kevin C Kobylinski
Joseph W Diclaro II
Fatorma K Bolay
Lawrence S Fakoli
Abdoulaye Diabaté
Roch K Dabiré
Roland W Bougma
Brian D Foy
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-417

Other articles of this Issue 1/2014

Malaria Journal 1/2014 Go to the issue