Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Indoor use of attractive toxic sugar bait (ATSB) to effectively control malaria vectors in Mali, West Africa

Authors: Whitney A Qualls, Günter C Müller, Sekou F Traore, Mohamed M Traore, Kristopher L Arheart, Seydou Doumbia, Yosef Schlein, Vasiliy D Kravchenko, Rui-De Xue, John C Beier

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Attractive toxic sugar bait (ATSB) solutions containing any gut toxins can be either sprayed on plants or used in simple bait stations to attract and kill sugar-feeding female and male mosquitoes. This field study in Mali demonstrates the effect of ATSB bait stations inside houses as a vector control method that targets and kills endophilic African malaria vectors.

Methods

The studies were conducted in five villages located near the River Niger, Mali. Baseline village-wide assessments of densities for female and male Anopheles gambiae sensu lato were performed by pyrethrum spray collections (PSC) in ten houses in each of five villages. To determine the rate of mosquito feeding on bait stations, one bait station per house containing attractive sugar bait (ASB) (without toxin) plus a food dye marker, was set up in ten houses in each of the five villages. PSC collections were conducted on the following day and the percentage of female and male mosquitoes that had fed was determined by visual inspection for the dye marker. Then, a 50-day field trial was done. In an experimental village, one bait station containing ATSB (1% boric acid active ingredient) was placed per bedroom (58 bedrooms), and indoor densities of female and male An. gambiae s.l. were subsequently determined by PSC, and female mosquitoes were age graded.

Results

In the five villages, the percentages of An. gambiae s.l. feeding inside houses on the non-toxic bait stations ranged from 28.3 to 53.1% for females and 36.9 to 78.3% for males. Following ATSB indoor bait station presentation, there was a significant reduction, 90% in female and 93% in male populations, of An. gambiae s.l. at the experimental village. A 3.8-fold decrease in the proportion of females that had undergone four or more gonotrophic cycles was recorded at the experimental village, compared to a 1.2-fold increase at the control village.

Conclusion

The field trial demonstrates that An. gambiae s.l. feed readily from ATSB bait stations situated indoors, leading to a substantial reduction in the proportion of older female mosquitoes. This study demonstrates that ATSB inside houses can achieve impressive malaria vector control in Africa.
Literature
1.
go back to reference WHO (2004) Global strategic framework for integrated vector management. World Health Organization, pp 1–12. WHO/CDS/CPE/PVC/2004 WHO (2004) Global strategic framework for integrated vector management. World Health Organization, pp 1–12. WHO/CDS/CPE/PVC/2004
2.
go back to reference WHO (2008) WHO position statement on integrated vector management. Wkly Epidemiol Rec 83:177 WHO (2008) WHO position statement on integrated vector management. Wkly Epidemiol Rec 83:177
3.
4.
go back to reference World Health Organization (2004) Malaria vector control and personal protection. World Health Organization, Geneva Switzerland, p 936. WHO Technical Report Series 2004 World Health Organization (2004) Malaria vector control and personal protection. World Health Organization, Geneva Switzerland, p 936. WHO Technical Report Series 2004
5.
go back to reference WHO (2008) Global malaria control and elimination: report of a technical review. World Health Organization, Geneva WHO (2008) Global malaria control and elimination: report of a technical review. World Health Organization, Geneva
6.
go back to reference Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot O et al (2012) Malaria resurgence: a systematic review and assessment of its causes. Malar J 11:122PubMedCentralPubMedCrossRef Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot O et al (2012) Malaria resurgence: a systematic review and assessment of its causes. Malar J 11:122PubMedCentralPubMedCrossRef
7.
go back to reference Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR (2013) Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J 12:56PubMedCentralPubMedCrossRef Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR (2013) Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J 12:56PubMedCentralPubMedCrossRef
8.
go back to reference Müller GC, Schlein Y (2006) Sugar questing mosquitoes in arid areas gather on scarce blossoms that can be used for control. Int J Parasitol 36:1077–1080PubMedCrossRef Müller GC, Schlein Y (2006) Sugar questing mosquitoes in arid areas gather on scarce blossoms that can be used for control. Int J Parasitol 36:1077–1080PubMedCrossRef
9.
go back to reference Müller GC, Schlein Y (2008) Efficacy of toxic sugar baits against adult cistern dwelling Anopheles claviger. Trans R Soc Trop Med Hyg 102:480–484PubMedCrossRef Müller GC, Schlein Y (2008) Efficacy of toxic sugar baits against adult cistern dwelling Anopheles claviger. Trans R Soc Trop Med Hyg 102:480–484PubMedCrossRef
10.
go back to reference Schlein Y, Müller GC (2008) An approach to mosquito control: using the dominant attraction of flowering Tamarix jordanis trees against Culex pipiens. J Med Entomol 45:384–390PubMedCrossRef Schlein Y, Müller GC (2008) An approach to mosquito control: using the dominant attraction of flowering Tamarix jordanis trees against Culex pipiens. J Med Entomol 45:384–390PubMedCrossRef
11.
go back to reference Müller GC, Kravchenko VD, Schlein Y (2008) Decline of Anopheles sergenti and Aedes caspius populations following presentation of attractive, toxic (Spinosad), sugar bait stations in an oasis. J Am Mosq Control Assoc 12:147–149CrossRef Müller GC, Kravchenko VD, Schlein Y (2008) Decline of Anopheles sergenti and Aedes caspius populations following presentation of attractive, toxic (Spinosad), sugar bait stations in an oasis. J Am Mosq Control Assoc 12:147–149CrossRef
12.
go back to reference Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S et al (2010) Successful field trial of attractive toxic sugar bait (ATSB) plant spraying methods against malaria vectors in the Anopheles gambiae complex in Mali, West Africa. Malar J 9:210PubMedCentralPubMedCrossRef Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S et al (2010) Successful field trial of attractive toxic sugar bait (ATSB) plant spraying methods against malaria vectors in the Anopheles gambiae complex in Mali, West Africa. Malar J 9:210PubMedCentralPubMedCrossRef
13.
go back to reference Müller GC, Junnila A, Schlein Y (2010) Effective control of adult Culex pipiens by spraying an attractive toxic sugar bait solution in the vegetation near larval habitats. J Med Entomol 47:63–66PubMedCrossRef Müller GC, Junnila A, Schlein Y (2010) Effective control of adult Culex pipiens by spraying an attractive toxic sugar bait solution in the vegetation near larval habitats. J Med Entomol 47:63–66PubMedCrossRef
14.
go back to reference Beier JC, Müller GC, Gu W, Arheart KL, Schlein Y (2012) Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malar J 11:31PubMedCentralPubMedCrossRef Beier JC, Müller GC, Gu W, Arheart KL, Schlein Y (2012) Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favoured sugar-source blossoms. Malar J 11:31PubMedCentralPubMedCrossRef
15.
go back to reference Gu W, Müller GC, Schlein Y, Novak RJ, Beier JC (2011) Natural plant sugar sources of Anopheles mosquitoes strongly impact malaria transmission potential. PLoS One 6:e15996PubMedCentralPubMedCrossRef Gu W, Müller GC, Schlein Y, Novak RJ, Beier JC (2011) Natural plant sugar sources of Anopheles mosquitoes strongly impact malaria transmission potential. PLoS One 6:e15996PubMedCentralPubMedCrossRef
16.
go back to reference Qualls WA, Xue RD, Revay EE, Allan SA, Müller GC (2012) Implications for operational control of adult mosquito production in cistern and wells in St. Augustine, FL using attractive sugar baits. Acta Trop 124:156–161CrossRef Qualls WA, Xue RD, Revay EE, Allan SA, Müller GC (2012) Implications for operational control of adult mosquito production in cistern and wells in St. Augustine, FL using attractive sugar baits. Acta Trop 124:156–161CrossRef
17.
go back to reference Naranjo DP, Qualls WA, Alimi TO, Roque DD, Samson DM, Arheart KC et al (2013) Evaluation of boric acid sugar baits against Aedes albopictus (Diptera: Culicidae) in tropical environments. Parasitol Res 112:1583–1587PubMedCrossRef Naranjo DP, Qualls WA, Alimi TO, Roque DD, Samson DM, Arheart KC et al (2013) Evaluation of boric acid sugar baits against Aedes albopictus (Diptera: Culicidae) in tropical environments. Parasitol Res 112:1583–1587PubMedCrossRef
18.
go back to reference Khallaayoune K, Qualls WA, Revay EE, Allan SA, Arheart KA, Kravchenko VD et al (2013) Attractive toxic sugar baits: control of mosquitoes with the low risk active ingredient dinotefuran and potential impacts on non-target organisms in Morocco. Environ Entomol 42:1040–1045PubMedCentralPubMedCrossRef Khallaayoune K, Qualls WA, Revay EE, Allan SA, Arheart KA, Kravchenko VD et al (2013) Attractive toxic sugar baits: control of mosquitoes with the low risk active ingredient dinotefuran and potential impacts on non-target organisms in Morocco. Environ Entomol 42:1040–1045PubMedCentralPubMedCrossRef
19.
go back to reference Revay EE, Müller GC, Qualls WA, Kline DL, Narnajo DP, Arheart KL et al (2014) Control of Aedes albopictus with attractive toxic sugar baits (ATSB) and potential impact on non-target organism in St. Augustine, Florida. Parasitol Res 113:73–79PubMedCentralPubMedCrossRef Revay EE, Müller GC, Qualls WA, Kline DL, Narnajo DP, Arheart KL et al (2014) Control of Aedes albopictus with attractive toxic sugar baits (ATSB) and potential impact on non-target organism in St. Augustine, Florida. Parasitol Res 113:73–79PubMedCentralPubMedCrossRef
20.
go back to reference Qualls WA, Müller GC, Revay EE, Allan SA, Arheart KL, Beier JC et al (2014) Evaluation of attractive toxic sugar baits (ATSB)—barrier control of vector and nuisance mosquitoes and its effect on non-target organisms in sub-tropical environments in Florida. Acta Trop 131:104–110PubMedCentralPubMedCrossRef Qualls WA, Müller GC, Revay EE, Allan SA, Arheart KL, Beier JC et al (2014) Evaluation of attractive toxic sugar baits (ATSB)—barrier control of vector and nuisance mosquitoes and its effect on non-target organisms in sub-tropical environments in Florida. Acta Trop 131:104–110PubMedCentralPubMedCrossRef
21.
go back to reference Fulcher A, Scott JM, Qualls WA, Müller GC, Xue RD (2014) Attractive toxic sugar baits mixed with pyriproxyfen sprayed on plants again adult and larval Aedes albopictus (Diptera: Culicidae). J Med Entomol 51:896–899PubMedCrossRef Fulcher A, Scott JM, Qualls WA, Müller GC, Xue RD (2014) Attractive toxic sugar baits mixed with pyriproxyfen sprayed on plants again adult and larval Aedes albopictus (Diptera: Culicidae). J Med Entomol 51:896–899PubMedCrossRef
22.
go back to reference Xue RD, Kline DL, Ali A, Barnard DR (2006) Application of boric acid baits to plant foliage for adult mosquito control. J Am Mosq Control Assoc 22:497–500PubMedCrossRef Xue RD, Kline DL, Ali A, Barnard DR (2006) Application of boric acid baits to plant foliage for adult mosquito control. J Am Mosq Control Assoc 22:497–500PubMedCrossRef
23.
go back to reference Enayati A, Hemingway J (2010) Malaria management: past, present, and future. Ann Rev Entomol 55:569–591CrossRef Enayati A, Hemingway J (2010) Malaria management: past, present, and future. Ann Rev Entomol 55:569–591CrossRef
24.
go back to reference Environmental Protection Agency (2014) Minimum risk pesticides. EPA.gov Environmental Protection Agency (2014) Minimum risk pesticides. EPA.gov
25.
go back to reference Allan SA (2011) Laboratory evaluation of mosquito susceptibility to insecticides combined with sucrose. J Vector Ecol 36:59–67PubMedCrossRef Allan SA (2011) Laboratory evaluation of mosquito susceptibility to insecticides combined with sucrose. J Vector Ecol 36:59–67PubMedCrossRef
26.
go back to reference Sogoba N, Vounatsou P, Bagayoko MM, Doumbia S, Dolo G, Gosoniu L et al (2007) The spatial distribution of Anopheles gambiae sensu stricto and Anopheles arabiensis (Diptera: Culicidae) in Mali. Geospat Health 1:213–222PubMedCrossRef Sogoba N, Vounatsou P, Bagayoko MM, Doumbia S, Dolo G, Gosoniu L et al (2007) The spatial distribution of Anopheles gambiae sensu stricto and Anopheles arabiensis (Diptera: Culicidae) in Mali. Geospat Health 1:213–222PubMedCrossRef
27.
go back to reference Dicko A, Mantel C, Kouriba B, Sagara I, Thera MA, Doumbia S et al (2005) Season, fever prevalence and pyrogenic threshold for malaria disease definition in an endemic area of Mali. Trop Med Int Health 10:550–556PubMedCrossRef Dicko A, Mantel C, Kouriba B, Sagara I, Thera MA, Doumbia S et al (2005) Season, fever prevalence and pyrogenic threshold for malaria disease definition in an endemic area of Mali. Trop Med Int Health 10:550–556PubMedCrossRef
28.
go back to reference Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S et al (2010) Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar J 9:262PubMedCentralPubMedCrossRef Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Bah S et al (2010) Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar J 9:262PubMedCentralPubMedCrossRef
29.
go back to reference Müller GC, Junnila A, Qualls WA, Revay EE, Kline DL, Allan S et al (2010) Control of Culex quinquefasciatus in a storm drain system in Florida using attractive toxic sugar baits. J Med Vet Entomol 24:346–351CrossRef Müller GC, Junnila A, Qualls WA, Revay EE, Kline DL, Allan S et al (2010) Control of Culex quinquefasciatus in a storm drain system in Florida using attractive toxic sugar baits. J Med Vet Entomol 24:346–351CrossRef
30.
go back to reference WHO (1975) Manual on practical entomology in malaria: part II—methods and techniques. World Health Organization Offset Publications No. 13, Geneva WHO (1975) Manual on practical entomology in malaria: part II—methods and techniques. World Health Organization Offset Publications No. 13, Geneva
31.
go back to reference Scott JA, Brogdon WG, Collins FH (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49:520–529PubMed Scott JA, Brogdon WG, Collins FH (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49:520–529PubMed
32.
go back to reference Gillies MT, DeMeillon B (1968) The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). Publication of the South Africa Institute of Med. Res. 1968, No. 54. Hortors Printers Johannesburg, South Africa Gillies MT, DeMeillon B (1968) The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). Publication of the South Africa Institute of Med. Res. 1968, No. 54. Hortors Printers Johannesburg, South Africa
33.
go back to reference Nunes RD, de Oliveira RL, Braz GR (2008) A novel method for measuring fructose ingestion by mosquitoes. J Vector Ecol 33:225PubMedCrossRef Nunes RD, de Oliveira RL, Braz GR (2008) A novel method for measuring fructose ingestion by mosquitoes. J Vector Ecol 33:225PubMedCrossRef
34.
go back to reference Detinova TS (1962) Age grouping methods in Diptera of medical importance. World Health Organization Monograph Series 47, Geneva, Switzerland Detinova TS (1962) Age grouping methods in Diptera of medical importance. World Health Organization Monograph Series 47, Geneva, Switzerland
35.
go back to reference Marshall JM, White MT, Chani AC, Schlein Y, Müller GC, Beier JC (2013) Quantifying the mosquito’s sweet tooth: modelling the effectiveness of attractive toxic sugar baits (ATSB) for malaria vector control. Malar J 12:291PubMedCentralPubMedCrossRef Marshall JM, White MT, Chani AC, Schlein Y, Müller GC, Beier JC (2013) Quantifying the mosquito’s sweet tooth: modelling the effectiveness of attractive toxic sugar baits (ATSB) for malaria vector control. Malar J 12:291PubMedCentralPubMedCrossRef
36.
go back to reference Stewart ZP, Oxborough RM, Tungus PK, Kirby MJ, Rowland MW, Irish SR (2013) Indoor application of attractive toxic sugar bait (ATSB) in combination with mosquito nets for control of pyrethroid-resistant mosquitoes. PLoS One 8:e84168PubMedCentralPubMedCrossRef Stewart ZP, Oxborough RM, Tungus PK, Kirby MJ, Rowland MW, Irish SR (2013) Indoor application of attractive toxic sugar bait (ATSB) in combination with mosquito nets for control of pyrethroid-resistant mosquitoes. PLoS One 8:e84168PubMedCentralPubMedCrossRef
37.
38.
go back to reference Vontas J, Moore S, Kleinschmidt I, Ranson H, Lindsay S, Lengeler C et al (2014) Framework for rapid assessment and adoption of new vector control tools. Trends Parasitol 30:191–204PubMedCrossRef Vontas J, Moore S, Kleinschmidt I, Ranson H, Lindsay S, Lengeler C et al (2014) Framework for rapid assessment and adoption of new vector control tools. Trends Parasitol 30:191–204PubMedCrossRef
Metadata
Title
Indoor use of attractive toxic sugar bait (ATSB) to effectively control malaria vectors in Mali, West Africa
Authors
Whitney A Qualls
Günter C Müller
Sekou F Traore
Mohamed M Traore
Kristopher L Arheart
Seydou Doumbia
Yosef Schlein
Vasiliy D Kravchenko
Rui-De Xue
John C Beier
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0819-8

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue