Household and maternal risk factors for malaria in pregnancy in a highly endemic area of Uganda: a prospective cohort study

Jaffer Okiring, Peter Olwoch, Abel Kakuru, Joseph Okou, Harriet Ochokoru, Tedy Andra Ochieng, Richard Kajubi, Moses R Kamya, Grant Dorsey, Lucy S Tusting, Jaffer Okiring, Peter Olwoch, Abel Kakuru, Joseph Okou, Harriet Ochokoru, Tedy Andra Ochieng, Richard Kajubi, Moses R Kamya, Grant Dorsey, Lucy S Tusting

Abstract

Background: Malaria in pregnancy is a major public health challenge, but its risk factors remain poorly understood in some settings. This study assessed the association between household and maternal characteristics and malaria among pregnant women in a high transmission area of Uganda.

Methods: A nested prospective study was conducted between 6th September 2016 and 5th December 2017 in Busia district. 782 HIV uninfected women were enrolled in the parent study with convenience sampling. Socioeconomic and house construction data were collected via a household survey after enrolment. Homes were classified as modern (plaster or cement walls, metal or wooden roof and closed eaves) or traditional (all other homes). Maternal and household risk factors were evaluated for three outcomes: (1) malaria parasitaemia at enrolment, measured by thick blood smear and qPCR, (2) malaria parasitaemia during pregnancy following initiation of IPTp, measured by thick blood smear and qPCR and (3) placental malaria measured by histopathology.

Results: A total of 753 of 782 women were included in the analysis. Most women had no or primary education (75%) and lived in traditional houses (77%). At enrolment, microscopic or sub-microscopic parasitaemia was associated with house type (traditional versus modern: adjusted risk ratio (aRR) 1.29, 95% confidence intervals 1.15-1.45, p < 0.001), level of education (primary or no education versus O-level or beyond: aRR 1.13, 95% confidence interval 1.02-1.24, p = 0.02), and gravidity (primigravida versus multigravida: aRR 1.10, 95% confidence interval 1.02-1.18, p = 0.009). After initiation of IPTp, microscopic or sub-microscopic parasitaemia was associated with wealth index (poorest versus least poor: aRR 1.24, 95% CI 1.10-1.39, p < 0.001), house type (aRR 1.14, 95% CI 1.01-1.28, p = 0.03), education level (aRR 1.19, 95% CI 1.06-1.34, p = 0.002) and gravidity (aRR 1.32, 95% CI 1.20-1.45, p < 0.001). Placental malaria was associated with gravidity (aRR 2.87, 95% CI 2.39-3.45, p < 0.001), but not with household characteristics.

Conclusions: In an area of high malaria transmission, primigravid women and those belonging to the poorest households, living in traditional homes and with the least education had the greatest risk of malaria during pregnancy.

Keywords: Area of high malaria endemicity; Malaria in pregnancy; Risk factors.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

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Fig. 1
Trial profile

References

    1. Walker PGT, 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–e467. doi: 10.1016/S2214-109X(14)70256-6.
    1. 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. doi: 10.1016/S1473-3099(07)70021-X.
    1. Eisele TP, Larsen DA, Anglewicz PA, Keating J, Yukich J, Bennett A, et al. Malaria prevention in pregnancy, birthweight, and neonatal mortality: a meta-analysis of 32 national cross-sectional datasets in Africa. Lancet Infect Dis. 2012;12:942–949. doi: 10.1016/S1473-3099(12)70222-0.
    1. Braun V, Rempis E, Schnack A, Decker S, Rubaihayo J, Tumwesigye NM, et al. Lack of effect of intermittent preventive treatment for malaria in pregnancy and intense drug resistance in western Uganda. Malar J. 2015;14:372. doi: 10.1186/s12936-015-0909-7.
    1. 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. doi: 10.1371/journal.pone.0073073.
    1. Tusting LS, Willey B, Lucas H, Thompson J, Toto Kafy H, Smith R, et al. Socioeconomic development as an intervention against malaria: a systematic review and meta-analysis. Lancet. 2013;382:834. doi: 10.1016/S0140-6736(13)60851-X.
    1. Tusting LS, Bottomley C, Gibson H, Kleinschmidt I, Tatem AJ, Lindsay S, et al. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med. 2017;14:e1002234. doi: 10.1371/journal.pmed.1002234.
    1. RBM/UNDP . Multisectoral action framework for malaria. Geneva: Roll Back Malaria/United Nations Development Programme; 2013.
    1. Fana SA, Bunza MDA, Anka SA, Imam AU, Nataala SU. Prevalence and risk factors associated with malaria infection among pregnant women in a semi-urban community of north-western Nigeria. Infect Dis Poverty. 2015;4:24. doi: 10.1186/s40249-015-0054-0.
    1. Valente B, Campos PA, de Rosário VE, Varandas L, Silveira H. Prevalence and risk factors of Plasmodium falciparum infections in pregnant women of Luanda, Angola. Trop Med Int Health. 2011;16:1206–1214. doi: 10.1111/j.1365-3156.2011.02830.x.
    1. Pell C, Straus L, Andrew E, Meñaca A, Pool R. Social and cultural factors affecting uptake of interventions for malaria in pregnancy in Africa: a systematic review of the qualitative research. PLoS One. 2011;6:e22452. doi: 10.1371/journal.pone.0022452.
    1. Mubyazi G, Bloch P, Kamugisha M, Kitua A, Ijumba J. Intermittent preventive treatment of malaria during pregnancy: a qualitative study of knowledge, attitudes and practices of district health managers, antenatal care staff and pregnant women in Korogwe District, North-Eastern Tanzania. Malar J. 2005;4:31. doi: 10.1186/1475-2875-4-31.
    1. Odongo CO, Bisaso RK, Byamugisha J, Obua C. Intermittent use of sulphadoxine-pyrimethamine for malaria prevention: a cross-sectional study of knowledge and practices among Ugandan women attending an urban antenatal clinic. Malar J. 2014;13:399. doi: 10.1186/1475-2875-13-399.
    1. Muhumuza E, Namuhani N, Balugaba BE, Namata J, Ekirapa Kiracho E. Factors associated with use of malaria control interventions by pregnant women in Buwunga subcounty, Bugiri District. Malar J. 2016;15:342. doi: 10.1186/s12936-016-1407-2.
    1. Hill J, Hoyt J, van Eijk AM, D’Mello-Guyett L, ter Kuile FO, Steketee R, et al. Factors affecting the delivery, access and use of interventions to prevent malaria in pregnancy in sub-Saharan Africa: a systematic review and meta-analysis. PLoS Med. 2013;10:e1001488. doi: 10.1371/journal.pmed.1001488.
    1. Sangare LR, Stergachis A, Brentlinger PE, Richardson BA, Staedke SG, Kiwuwa MS, et al. Determinants of use of intermittent preventive treatment of malaria in pregnancy: Jinja, Uganda. PLoS One. 2010;5:e15066. doi: 10.1371/journal.pone.0015066.
    1. Launiala A, Kulmala T. The importance of understanding the local context: women’s perceptions and knowledge concerning malaria in pregnancy in rural Malawi. Acta Trop. 2006;98:111–117. doi: 10.1016/j.actatropica.2005.12.008.
    1. Mbonye AK, Neema S, Magnussen P. Preventing malaria in pregnancy: a study of perceptions and policy implications in Mukono district, Uganda. Health Policy Plan. 2006;21:17–26. doi: 10.1093/heapol/czj002.
    1. Adam I, Khamis AH, Elbashir MI. Prevalence and risk factors for Plasmodium falciparum malaria in pregnant women of eastern Sudan. Malar J. 2005;4:18. doi: 10.1186/1475-2875-4-18.
    1. Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke RF. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg. 2005;72:236–242. doi: 10.4269/ajtmh.2005.72.236.
    1. Woodburn PW, Muhangi L, Hillier S, Ndibazza J, Namujju PB, Kizza M, et al. Risk factors for helminth, malaria, and HIV infection in pregnancy in Entebbe, Uganda. PLoS Neglect Trop Dis. 2009;3:e473. doi: 10.1371/journal.pntd.0000473.
    1. Muhindo MK, Kakuru A, Natureeba P, Awori P, Olwoch P, Ategeka J, et al. Reductions in malaria in pregnancy and adverse birth outcomes following indoor residual spraying of insecticide in Uganda. Malar J. 2016;15:437. doi: 10.1186/s12936-016-1489-x.
    1. Kajubi R, Ochieng T, Kakuru A, Jagannathan P, Nakalembe M, Ruel T, et al. Monthly sulfadoxine-pyrimethamine versus dihydroartemisininpiperaquine for intermittent preventive treatment of malaria in pregnancy: a randomized controlled trial. Lancet. 2019;393:1428–1439. doi: 10.1016/S0140-6736(18)32224-4.
    1. Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med. 2015;12:e1001788. doi: 10.1371/journal.pmed.1001788.
    1. Wanzira H, Tusting LS, Arinaitwe E, Katureebe A, Maxwell K, Rek J, et al. Mind the gap: house structure and the risk of malaria in Uganda. PLoS ONE. 2015;10:e0117396. doi: 10.1371/journal.pone.0117396.
    1. van Eijk AM, Hill J, Noor AM, Snow RW, ter Kuile FO. Prevalence of malaria infection in pregnant women compared with children for tracking malaria transmission in sub-Saharan Africa: a systematic review and meta-analysis. Lancet Glob Health. 2015;3:e617–e628. doi: 10.1016/S2214-109X(15)00049-2.
    1. Jagannathan P, Kakuru A, Okiring J, Muhindo MK, Natureeba P, Nakalembe M, et al. Dihydroartemisinin-piperaquine for intermittent preventive treatment of malaria during pregnancy and risk of malaria in early childhood: a randomized controlled trial. PLoS Med. 2018;15:e1002606. doi: 10.1371/journal.pmed.1002606.
    1. WHO . World malaria report. Geneva: World Health Organization; 2018.
    1. Tusting LS, Rek J, Arinaitwe E, Staedke SG, Kamya MR, Cano J, et al. Why is malaria associated with poverty? Findings from a cohort study in rural Uganda. Infect Dis Poverty. 2016;5:78. doi: 10.1186/s40249-016-0164-3.
    1. Kirby MJ, Green C, Milligan P, Sismanidis C, Jasseh M, Conway DJ, et al. Risk factors for house-entry by malaria vectors in a rural town and satellite villages in The Gambia. Malar J. 2008;7:2. doi: 10.1186/1475-2875-7-2.
    1. Rek JC, Alegana V, Arinaitwe E, Cameron E, Kamya MR, Katureebe A, et al. Rapid improvements to rural Ugandan housing and their association with malaria from intense to reduced transmission: a cohort study. Lancet Planet Health. 2018;2:e83–e94. doi: 10.1016/S2542-5196(18)30010-X.
    1. Njau JD, Stephenson R, Menon MP, Kachur SP, McFarland DA. Investigating the important correlates of maternal education and childhood malaria infections. Am J Trop Med Hyg. 2014;91:509–519. doi: 10.4269/ajtmh.13-0713.
    1. Wanzira H, Katamba H, Okullo AE, Agaba B, Kasule M, Rubahika D. Factors associated with malaria parasitaemia among children under 5 years in Uganda: a secondary data analysis of the 2014 Malaria Indicator Survey dataset. Malar J. 2017;16:191. doi: 10.1186/s12936-017-1847-3.
    1. de Castro MC, Fisher MG. Is malaria illness among young children a cause or a consequence of low socioeconomic status? Evidence from the united Republic of Tanzania. Malar J. 2012;11:161. doi: 10.1186/1475-2875-11-161.

Source: PubMed

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