Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Reductions in malaria in pregnancy and adverse birth outcomes following indoor residual spraying of insecticide in Uganda

Authors: Mary K. Muhindo, Abel Kakuru, Paul Natureeba, Patricia Awori, Peter Olwoch, John Ategeka, Patience Nayebare, Tamara D. Clark, Atis Muehlenbachs, Michelle Roh, Betty Mpeka, Bryan Greenhouse, Diane V. Havlir, Moses R. Kamya, Grant Dorsey, Prasanna Jagannathan

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Indoor residual spraying of insecticide (IRS) is a key intervention for reducing the burden of malaria in Africa. However, data on the impact of IRS on malaria in pregnancy and birth outcomes is limited.

Methods

An observational study was conducted within a trial of intermittent preventive therapy during pregnancy in Tororo, Uganda. Women were enrolled at 12–20 weeks of gestation between June and October 2014, provided with insecticide-treated bed nets, and followed through delivery. From December 2014 to February 2015, carbamate-containing IRS was implemented in Tororo district for the first time. Exact spray dates were collected for each household. The exposure of interest was the proportion of time during a woman’s pregnancy under protection of IRS, with three categories of protection defined: no IRS protection, >0–20 % IRS protection, and 20–43 % IRS protection. Outcomes assessed included malaria incidence and parasite prevalence during pregnancy, placental malaria, low birth weight (LBW), pre-term delivery, and fetal/neonatal deaths.

Results

Of 289 women followed, 134 had no IRS protection during pregnancy, 90 had >0–20 % IRS protection, and 65 had >20–43 % protection. During pregnancy, malaria incidence (0.49 vs 0.10 episodes ppy, P = 0.02) and parasite prevalence (20.0 vs 8.9 %, P < 0.001) were both significantly lower after IRS. At the time of delivery, the prevalence of placental parasitaemia was significantly higher in women with no IRS protection (16.8 %) compared to women with 0–20 % (1.1 %, P = 0.001) or >20–43 % IRS protection (1.6 %, P = 0.006). Compared to women with no IRS protection, those with >20–43 % IRS protection had a lower risk of LBW (20.9 vs 3.1 %, P = 0.002), pre-term birth (17.2 vs 1.5 %, P = 0.006), and fetal/neonatal deaths (7.5 vs 0 %, P = 0.03).

Conclusion

In this setting, IRS was temporally associated with lower malaria parasite prevalence during pregnancy and at delivery, and improved birth outcomes. IRS may represent an important tool for combating malaria in pregnancy and for improving birth outcomes in malaria-endemic settings.
Trial Registration Current Controlled Trials Identifier NCT02163447
Appendix
Available only for authorised users
Literature
1.
go back to reference Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med. 2010;7:e1000221.CrossRefPubMedPubMedCentral Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med. 2010;7:e1000221.CrossRefPubMedPubMedCentral
2.
go back to reference Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.CrossRefPubMed
3.
go back to reference Walker PG, ter Kuile FO, Garske T, Menendez C, Ghani AC. Estimated risk of placental infection and low birthweight attributable to Plasmodium falciparum malaria in Africa in 2010: a modelling study. Lancet Glob Health. 2014;2:e460–7.CrossRefPubMed Walker PG, ter Kuile FO, Garske T, Menendez C, Ghani AC. Estimated risk of placental infection and low birthweight attributable to Plasmodium falciparum malaria in Africa in 2010: a modelling study. Lancet Glob Health. 2014;2:e460–7.CrossRefPubMed
4.
go back to reference WHO. World Malaria Report. Geneva. Switzerland: World Health Organization; 2015. p. 2015. WHO. World Malaria Report. Geneva. Switzerland: World Health Organization; 2015. p. 2015.
5.
go back to reference Arinaitwe E, Ades V, Walakira A, Ninsiima B, Mugagga O, Patil TS, et al. Intermittent preventive therapy with sulfadoxine-pyrimethamine for malaria in pregnancy: a cross-sectional study from Tororo, Uganda. PLoS One. 2013;8:e73073.CrossRefPubMedPubMedCentral Arinaitwe E, Ades V, Walakira A, Ninsiima B, Mugagga O, Patil TS, et al. Intermittent preventive therapy with sulfadoxine-pyrimethamine for malaria in pregnancy: a cross-sectional study from Tororo, Uganda. PLoS One. 2013;8:e73073.CrossRefPubMedPubMedCentral
6.
go back to reference Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ. Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol. 2013;27:276–83.CrossRefPubMed Mawejje HD, Wilding CS, Rippon EJ, Hughes A, Weetman D, Donnelly MJ. Insecticide resistance monitoring of field-collected Anopheles gambiae s.l. populations from Jinja, eastern Uganda, identifies high levels of pyrethroid resistance. Med Vet Entomol. 2013;27:276–83.CrossRefPubMed
7.
go back to reference Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, Müller P. Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med Hyg. 2009;103:1121–6.CrossRefPubMed Ramphul U, Boase T, Bass C, Okedi LM, Donnelly MJ, Müller P. Insecticide resistance and its association with target-site mutations in natural populations of Anopheles gambiae from eastern Uganda. Trans R Soc Trop Med Hyg. 2009;103:1121–6.CrossRefPubMed
8.
go back to reference Verhaeghen K, Van Bortel W, Trung HD, Sochantha T, Keokenchanh K, Coosemans M. Knockdown resistance in Anopheles vagus, An. sinensis, An. paraliae and An. peditaeniatus populations of the Mekong region. Parasit Vectors. 2010;3:59.CrossRefPubMedPubMedCentral Verhaeghen K, Van Bortel W, Trung HD, Sochantha T, Keokenchanh K, Coosemans M. Knockdown resistance in Anopheles vagus, An. sinensis, An. paraliae and An. peditaeniatus populations of the Mekong region. Parasit Vectors. 2010;3:59.CrossRefPubMedPubMedCentral
9.
go back to reference ter Kuile FO, van Eijk AM, Filler SJ. Effect of sulfadoxine-pyrimethamine resistance on the efficacy of intermittent preventive therapy for malaria control during pregnancy: a systematic review. JAMA. 2007;297:2603–16.CrossRefPubMed ter Kuile FO, van Eijk AM, Filler SJ. Effect of sulfadoxine-pyrimethamine resistance on the efficacy of intermittent preventive therapy for malaria control during pregnancy: a systematic review. JAMA. 2007;297:2603–16.CrossRefPubMed
10.
go back to reference Bukirwa H, Yau V, Kigozi R, Filler S, Quick L, Lugemwa M, et al. Assessing the impact of indoor residual spraying on malaria morbidity using a sentinel site surveillance system in Western Uganda. Am J Trop Med Hyg. 2009;81:611–4.CrossRefPubMed Bukirwa H, Yau V, Kigozi R, Filler S, Quick L, Lugemwa M, et al. Assessing the impact of indoor residual spraying on malaria morbidity using a sentinel site surveillance system in Western Uganda. Am J Trop Med Hyg. 2009;81:611–4.CrossRefPubMed
11.
go back to reference Zhou G, Githeko AK, Minakawa N, Yan G. Community-wide benefits of targeted indoor residual spray for malaria control in the western Kenya highland. Malar J. 2010;9:67.CrossRefPubMedPubMedCentral Zhou G, Githeko AK, Minakawa N, Yan G. Community-wide benefits of targeted indoor residual spray for malaria control in the western Kenya highland. Malar J. 2010;9:67.CrossRefPubMedPubMedCentral
12.
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
13.
go back to reference Skarbinski J, Mwandama D, Wolkon A, Luka M, Jafali J, Smith A, et al. Impact of indoor residual spraying with lambda-cyhalothrin on malaria parasitemia and anemia prevalence among children less than 5 years of age in an area of intense, year-round transmission in Malawi. Am J Trop Med Hyg. 2012;86:997–1004.CrossRefPubMedPubMedCentral Skarbinski J, Mwandama D, Wolkon A, Luka M, Jafali J, Smith A, et al. Impact of indoor residual spraying with lambda-cyhalothrin on malaria parasitemia and anemia prevalence among children less than 5 years of age in an area of intense, year-round transmission in Malawi. Am J Trop Med Hyg. 2012;86:997–1004.CrossRefPubMedPubMedCentral
14.
go back to reference Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS One. 2012;7:e42857.CrossRefPubMedPubMedCentral Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS One. 2012;7:e42857.CrossRefPubMedPubMedCentral
15.
go back to reference Hamel MJ, Otieno P, Bayoh N, Kariuki S, Were V, Marwanga D, et al. The combination of indoor residual spraying and insecticide-treated nets provides added protection against malaria compared with insecticide-treated nets alone. Am J Trop Med Hyg. 2011;85:1080–6.CrossRefPubMedPubMedCentral Hamel MJ, Otieno P, Bayoh N, Kariuki S, Were V, Marwanga D, et al. The combination of indoor residual spraying and insecticide-treated nets provides added protection against malaria compared with insecticide-treated nets alone. Am J Trop Med Hyg. 2011;85:1080–6.CrossRefPubMedPubMedCentral
16.
go back to reference West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Indoor residual spraying in combination with insecticide-treated nets compared to insecticide-treated nets alone for protection against malaria: a cluster randomised trial in Tanzania. PLoS Med. 2014;11(4):e1001630.CrossRefPubMedPubMedCentral West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, et al. Indoor residual spraying in combination with insecticide-treated nets compared to insecticide-treated nets alone for protection against malaria: a cluster randomised trial in Tanzania. PLoS Med. 2014;11(4):e1001630.CrossRefPubMedPubMedCentral
17.
go back to reference Gimnig JE, Otieno P, Were V, Marwanga D, Abong’o D, Wiegand R, et al. The effect of indoor residual spraying on the prevalence of malaria parasite infection, clinical malaria and anemia in an area of perennial transmission and moderate coverage of insecticide treated nets in Western Kenya. PLoS One. 2016;11:e0145282.CrossRefPubMedPubMedCentral Gimnig JE, Otieno P, Were V, Marwanga D, Abong’o D, Wiegand R, et al. The effect of indoor residual spraying on the prevalence of malaria parasite infection, clinical malaria and anemia in an area of perennial transmission and moderate coverage of insecticide treated nets in Western Kenya. PLoS One. 2016;11:e0145282.CrossRefPubMedPubMedCentral
18.
go back to reference Hamainza B, Sikaala CH, Moonga HB, Chanda J, Chinula D, Mwenda M, et al. Incremental impact upon malaria transmission of supplementing pyrethroid-impregnated long-lasting insecticidal nets with indoor residual spraying using pyrethroids or the organophosphate, pirimiphos methyl. Malar J. 2016;15:100.CrossRefPubMedPubMedCentral Hamainza B, Sikaala CH, Moonga HB, Chanda J, Chinula D, Mwenda M, et al. Incremental impact upon malaria transmission of supplementing pyrethroid-impregnated long-lasting insecticidal nets with indoor residual spraying using pyrethroids or the organophosphate, pirimiphos methyl. Malar J. 2016;15:100.CrossRefPubMedPubMedCentral
19.
go back to reference Pinder M, Jawara M, Jarju LB, Salami K, Jeffries D, Adiamoh M, et al. Efficacy of indoor residual spraying with dichlorodiphenyltrichloroethane against malaria in Gambian communities with high usage of long-lasting insecticidal mosquito nets: a cluster-randomised controlled trial. Lancet. 2015;385:1436–46.CrossRefPubMed Pinder M, Jawara M, Jarju LB, Salami K, Jeffries D, Adiamoh M, et al. Efficacy of indoor residual spraying with dichlorodiphenyltrichloroethane against malaria in Gambian communities with high usage of long-lasting insecticidal mosquito nets: a cluster-randomised controlled trial. Lancet. 2015;385:1436–46.CrossRefPubMed
20.
go back to reference Lines J, Kleinschmidt I. Is malaria control better with both treated nets and spraying? Lancet. 2015;385:1375–7.CrossRefPubMed Lines J, Kleinschmidt I. Is malaria control better with both treated nets and spraying? Lancet. 2015;385:1375–7.CrossRefPubMed
21.
go back to reference Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92:903–12.CrossRefPubMedPubMedCentral Kamya MR, Arinaitwe E, Wanzira H, Katureebe A, Barusya C, Kigozi SP, et al. Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control. Am J Trop Med Hyg. 2015;92:903–12.CrossRefPubMedPubMedCentral
22.
go back to reference Kakuru A, Jagannathan P, Muhindo MK, Natureeba P, Awori P, Nakalembe M, et al. Dihydroartemisinin–piperaquine for the prevention of malaria in pregnancy. N Engl J Med. 2016;374:928–39.CrossRefPubMed Kakuru A, Jagannathan P, Muhindo MK, Natureeba P, Awori P, Nakalembe M, et al. Dihydroartemisinin–piperaquine for the prevention of malaria in pregnancy. N Engl J Med. 2016;374:928–39.CrossRefPubMed
25.
go back to reference Hopkins H, Gonzalez IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208:645–52.CrossRefPubMedPubMedCentral Hopkins H, Gonzalez IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208:645–52.CrossRefPubMedPubMedCentral
26.
go back to reference Muehlenbachs A, Fried M, McGready R, Harrington WE, Mutabingwa TK, Nosten F, et al. A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis. 2010;202:1608–16.CrossRefPubMedPubMedCentral Muehlenbachs A, Fried M, McGready R, Harrington WE, Mutabingwa TK, Nosten F, et al. A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis. 2010;202:1608–16.CrossRefPubMedPubMedCentral
27.
go back to reference Mbonye AK, Birungi J, Yanow SK, Shokoples S, Malamba S, Alifrangis M, et al. Prevalence of Plasmodium falciparum resistance markers to sulfadoxine-pyrimethamine among pregnant women receiving intermittent preventive treatment for malaria in Uganda. Antimicrob Agents Chemother. 2015;59:5475–82.CrossRefPubMedPubMedCentral Mbonye AK, Birungi J, Yanow SK, Shokoples S, Malamba S, Alifrangis M, et al. Prevalence of Plasmodium falciparum resistance markers to sulfadoxine-pyrimethamine among pregnant women receiving intermittent preventive treatment for malaria in Uganda. Antimicrob Agents Chemother. 2015;59:5475–82.CrossRefPubMedPubMedCentral
28.
go back to reference Muehlenbachs A, Nabasumba C, McGready R, Turyakira E, Tumwebaze B, Dhorda M, et al. Artemether-lumefantrine to treat malaria in pregnancy is associated with reduced placental haemozoin deposition compared to quinine in a randomized controlled trial. Malar J. 2012;11:150.CrossRefPubMedPubMedCentral Muehlenbachs A, Nabasumba C, McGready R, Turyakira E, Tumwebaze B, Dhorda M, et al. Artemether-lumefantrine to treat malaria in pregnancy is associated with reduced placental haemozoin deposition compared to quinine in a randomized controlled trial. Malar J. 2012;11:150.CrossRefPubMedPubMedCentral
29.
go back to reference Piso B, Zechmeister-Koss I, Winkler R. Antenatal interventions to reduce preterm birth: an overview of cochrane systematic reviews. BMC Res Notes. 2014;7:265.CrossRefPubMedPubMedCentral Piso B, Zechmeister-Koss I, Winkler R. Antenatal interventions to reduce preterm birth: an overview of cochrane systematic reviews. BMC Res Notes. 2014;7:265.CrossRefPubMedPubMedCentral
30.
go back to reference Iams JD, Romero R, Culhane JF, Goldenberg RL. Primary, secondary, and tertiary interventions to reduce the morbidity and mortality of preterm birth. Lancet. 2008;371:164–75.CrossRefPubMed Iams JD, Romero R, Culhane JF, Goldenberg RL. Primary, secondary, and tertiary interventions to reduce the morbidity and mortality of preterm birth. Lancet. 2008;371:164–75.CrossRefPubMed
31.
go back to reference WHO. WHO recommendations on interventions to improve preterm birth outcomes. Geneva: World Health Organization; 2015. WHO. WHO recommendations on interventions to improve preterm birth outcomes. Geneva: World Health Organization; 2015.
32.
go back to reference Cottrell G, Moussiliou A, Luty AJ, Cot M, Fievet N, Massougbodji A, et al. Submicroscopic Plasmodium falciparum infections are associated with maternal anemia, premature births, and low birth weight. Clin Infect Dis. 2015;60:1481–8.PubMed Cottrell G, Moussiliou A, Luty AJ, Cot M, Fievet N, Massougbodji A, et al. Submicroscopic Plasmodium falciparum infections are associated with maternal anemia, premature births, and low birth weight. Clin Infect Dis. 2015;60:1481–8.PubMed
33.
go back to reference Desai M, Gutman J, L’Lanziva A, Otieno K, Juma E, Kariuki S, et al. Intermittent screening and treatment or intermittent preventive treatment with dihydroartemisinin-piperaquine versus intermittent preventive treatment with sulfadoxine-pyrimethamine for the control of malaria during pregnancy in western Kenya: an open-label, three-group, randomised controlled superiority trial. Lancet. 2015;386:2507–19.CrossRefPubMed Desai M, Gutman J, L’Lanziva A, Otieno K, Juma E, Kariuki S, et al. Intermittent screening and treatment or intermittent preventive treatment with dihydroartemisinin-piperaquine versus intermittent preventive treatment with sulfadoxine-pyrimethamine for the control of malaria during pregnancy in western Kenya: an open-label, three-group, randomised controlled superiority trial. Lancet. 2015;386:2507–19.CrossRefPubMed
34.
go back to reference Borchert JN, Eisen RJ, Atiku LA, Delorey MJ, Mpanga JT, Babi N, et al. Efficacy of indoor residual spraying using lambda-cyhalothrin for controlling nontarget vector fleas (Siphonaptera) on commensal rats in a plague endemic region of northwestern Uganda. J Med Entomol. 2012;49:1027–34.CrossRefPubMed Borchert JN, Eisen RJ, Atiku LA, Delorey MJ, Mpanga JT, Babi N, et al. Efficacy of indoor residual spraying using lambda-cyhalothrin for controlling nontarget vector fleas (Siphonaptera) on commensal rats in a plague endemic region of northwestern Uganda. J Med Entomol. 2012;49:1027–34.CrossRefPubMed
Metadata
Title
Reductions in malaria in pregnancy and adverse birth outcomes following indoor residual spraying of insecticide in Uganda
Authors
Mary K. Muhindo
Abel Kakuru
Paul Natureeba
Patricia Awori
Peter Olwoch
John Ategeka
Patience Nayebare
Tamara D. Clark
Atis Muehlenbachs
Michelle Roh
Betty Mpeka
Bryan Greenhouse
Diane V. Havlir
Moses R. Kamya
Grant Dorsey
Prasanna Jagannathan
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1489-x

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.