Skip to main content
Download PDF

Prevalence and factors associated with placental malaria in Lira District, Northern Uganda: a cross-sectional study

Malaria Journal volume 23, Article number: 360 (2024) Cite this article

Abstract

Background

Malaria has a stable perennial transmission across Uganda. Placental malaria is associated with adverse maternal, fetal, and neonatal outcomes. The factors associated with placental malaria are poorly understood in the study setting. The aim of the study was to assess the prevalence of placental malaria and to determine its associated factors among parturient women in Lira District, Uganda.

Methods

This was a cross-sectional study among 366 pregnant women who delivered at Lira Regional Referral Hospital. Data were collected from December 2018 to February 2019 using an interviewer-administered questionnaire. The variables were socio-demographic, obstetric characteristics, and malaria preventive practices. Standard Diagnostic Bioline Rapid Diagnostic Tests were used to detect placental malaria present in placental blood. Microscopy was used to quantify the grade of placental malaria parasitaemia. Logistic regression was used to assess factors associated with placental malaria.

Results

The mean age of the participants was 25.34 years (standard deviation [SD] 5.73). The prevalence of placental malaria was [4.4% (16/366) 95% CI (2.5 to 7.0)]. Of these, only 7/16 were positive on microscopy, with 2/7 having moderate parasitemia and 5/7 having mild parasitaemia. Women aged less than 20 years [AOR 3.48, 95% CI (1.13 to 10.72)], and those not taking iron supplements during pregnancy [AOR = 3.55, 95% CI (1.02 to 12.31)] were associated with an increased likelihood of having placental malaria.

Conclusion

The prevalence of placental malaria was low in this setting. This may have reflected the low malaria transmission rates following intensive indoor residual spraying. Placental malaria infection was associated with younger age and not taking iron supplements during pregnancy. Public health measures need to scale up and emphasise adherence to malaria preventive measures during pregnancy especially among teenage mothers.

Background

In Uganda, a stable malaria transmission occurs in 95% of the geographical area [1]. The second highest malaria transmission intensity worldwide has been reported in Northern Uganda [2]. In malaria endemic areas, pregnant women are more likely to suffer from severe malaria compared to the general population [3]. Pregnant women have a heightened risk of developing maternal anaemia, cerebral malaria and complications of malaria in pregnancy [4]. In addition, malaria in pregnancy is associated with an increased risk of developing adverse fetal outcomes such as spontaneous abortions, stillbirth, preterm birth, low birth weight and congenital malaria [4,5,6]. Maternal anaemia accounts for 10,000 maternal deaths, while low birth weight alone is reported to cause 200,000 neonatal deaths globally [4].

During pregnancy, physiological immune suppression occurs, and cell mediated immune response is reduced [4, 7]. In women living in malaria-endemic regions, and therefore have a degree of immunity to malaria by the time they become pregnant, the pregnancy-suppressed immune response enables the malaria parasite to survive [4, 7]. Plasmodium falciparum-infected red cells attach to the placenta, thus avoid spleen clearance and exposure to host immune responses [4, 7]. This triggers a cascade of inflammatory events which damage the placenta [7]. Consequently, placental insufficiency occurs hence intrauterine growth restriction, preterm delivery and low birth weight [7].

Uganda is one of the countries in the sub-Saharan region with the highest burden of malaria [8]. As such, Uganda adopted the three-pronged approach recommended by the World Health Organization to prevent malaria in pregnancy including the use of intermittent preventive treatment in pregnancy with sulfadoxine–pyrimethamine (IPT-SP), use of long-lasting insecticidal nets (LLINs), and effective case management of malaria [4, 9]. However, the coverage of these malaria preventive practices are sub-optimal and this increases the risk of malaria in pregnancy alongside other factors such as poor IPT-SP adherence and parasite resistance [10]. Despite the high (95%) attendance of antenatal care [11], only 41% of women received at least three doses of IPT-SP during pregnancy, while 65% of pregnant women used LLIN in 2019 [1]. From 2006 to 2021, when the indoor residual spraying (IRS) practice was implemented in the selected regions in Uganda [12], only 10% of the households had IRS [1]. In Northern Uganda, where the IRS campaign was intensified, indoor residual spraying was done in 57% of all the households [1, 12].

In Uganda, a number of studies have attempted to study the factors associated with placental malaria [13,14,15]. These studies were mostly done from areas of low and high intensity of malaria transmission [13,14,15]. The study was conducted in a setting of moderate intensity of malaria transmission. The increasing use of strategies for malaria prevention during pregnancy may change the reported prevalence of placental malaria. The emerging malaria parasite resistance trends and non-adherence to anti-malarials may influence the traditionally-known factors associated with placental malaria [16]. The purpose of this study was to determine the prevalence and the factors associated with placental malaria among pregnant women at Lira Regional Referral Hospital.

Methods

Study design and study setting

This was a cross-sectional study conducted in Lira Regional Referral Hospital. The hospital is located in the central business area of Lira district. The district is located in Northern Uganda which is approximately 342 km by road North of Kampala, the capital city of Uganda.

Lira district has a tropical rainfall pattern which is bimodal in nature with two rainy seasons [17]. The two rainy seasons start from the months of March to June and August to November, while the dry season starts in December to February and the month of July [17]. The malaria transmission rates peaks following the rainy season in the months of May and November [17]. The study was conducted from December 2018 to February 2019. Although the highest malaria transmission rates in the world have been observed in Apac District in Northern Uganda with an entolomolical inoculation rate of more than 1500 infective bites a year, Northern Uganda as a region is a malaria mesoendemic area [1]. This region has a prevalence of malaria of 20% in children of less than 10 years [18]. Plasmodium falciparum is the predominant malaria parasites, and Anopheles funestus is the main vector [19].

Study population, sampling and sample size

The study was conducted among pregnant women who came to give birth in Lira Regional Referral Hospital. Women in the first stage of labor were recruited in the study after obtaining written informed consent. Women who were critically ill and those who presented to the maternity ward in the second and third stage of labour were excluded from the study.

The study sample size was 366 women which was determined using the Cochran formula. The 39% prevalence of placental malaria from a study in Tanzania was used to calculate the study sample size using 5% precision estimate and Z-score of 1.96 for the 95% confidence interval [11]. Consecutive sampling method was used to select study participants.

Data collection procedure

Upon admission for delivery at Lira Regional Referral Hospital, the interviewer-administered paper based questionnaires were used to collect the independent variables in the study which included socio-demographic factors, obstetric factors, and malaria preventive practices. The age of a woman (> 20 or < 20 years), marital status (married/non-married), religion, ethnicity, level of education (< primary/ > secondary), occupation (employed/unemployed), area of residence (rural/urban), type of house (temporary/semipermanent or permanent) and fuel for cooking (charcoal/wood) were the corresponding socio-demographic variables. The malaria preventive practices included the use of IPT-SP (yes/no), number of IPT-SP doses (< 3/ > 2), dose interval of last IPT-SP dose from delivery (1/ ≥ 2 months), concomitant use of antimalarial drugs (yes/no) and directly observed therapy IPT-SP (yes/no) were extracted from the antenatal card, while use of bed net (yes/no), type of bed (LLIN/ordinary net), duration of bed net use (< 1/ > 1 year) and indoor residual spraying (yes/no) were collected from self-reports. The obstetric characteristics collected included parity (1–2/ ≥ 3, gestational age at delivery, iron supplementation, number of antenatal care (ANC) visits (< 4/ > 4 visits), ANC attendance (yes/no), the timing of first ANC (< 20/ > 20 weeks), history of malaria during pregnancy (yes/no), HIV status (yes/no) and iron supplementation (yes/no). Following delivery, a sample of placental blood was taken for malaria testing.

Process of sample collection

The placenta prick method was used to collect the placental blood [20]. The placental blood was collected immediately within the first 10 min after the placenta had been delivered. The placental blood, one to two millilitres, was aspirated from the center of the placenta along the maternal side of the placenta. The blood sample was stored in the Ethylenediaminetetraacetic acid sterile collection tube. The blood sample was labelled to correspond with the participant identification number on the questionnaire. The samples were then taken to the laboratory for sample processing.

Sample processing

The rapid diagnostic test (RDT) was used to diagnose placental malaria, while microscopy was used to quantify the parasitaemia of placental malaria infection. The RDT is an accurate proxy to diagnose placental malaria [21, 22]. Although placental histology is considered the gold standard for diagnosing placental malaria [23], RDT was used for practical reasons [4, 21, 22]. In a resource limited settings with a shortage of expertise and equipment required in microscopy [4], evidence has shown RDTs to be more superior than microscopy in detecting malaria in pregnancy [21, 22]. Microscopy are often limited by the low placental densities that tend to occur in pregnancy which compromise their accuracy [23]. Given the accuracy of RDTs [23], previous studies have also used RDTs as the end point for defining malaria in pregnancy [15, 24]. In this study, the SD Bioline (Ref: 05FK60) RDT was used to test for placental malaria infection. The RDT detects both the histidine rich protein 2 antigen specific for P. falciparum and the pan-lactate dehydrogenase antigen found in all Plasmodium species [21]. The RDT manufacturer’s instructions were strictly followed for testing for malaria. The RDT result was then entered into the questionnaire. The positive RDT samples were then subjected for microscopy to grade the parasitaemia of placental malaria.

The thick smear of placental blood was prepared to quantify the parasite density [25]. The smears were fixed in methanol for 5 s, then stained with 5% Giemsa for 30 min [25]. After staining, the blood smear was examined under the × 100 objective lens. The result was considered positive when the asexual forms of malaria parasites were observed [25]. Based on the standard criterion of classifying severe malaria in the setting, the degree of parasitaemia was graded as mild (1–999/μL), moderate (1000–9999/μL), and severe (> 10,000) [25]. The result was considered negative after a thorough examination of 100 fields was made without observation of the parasites [25]. The microscopy smear findings were interpreted by two qualified laboratory technicians. A third independent laboratory technician read the slides when a discrepancy occurred between the two readers. The study considered the test findings when the two laboratory technicians provided the same reading of the test including whether the test was negative or positive and the degree of parasitaemia.

Statistical analysis

The data for the study were entered and analysed using SPSS (version 16.0). The mean and standard deviation was used to describe the age of the study participants. Frequencies and percentages were used to describe the categorical variables in the study. The prevalence of placental malaria was determined by dividing the number of women with a positive finding for placental malaria by the total sample. The factors likely to be associated with placental malaria were identified from literature [26, 27]. Bivariable logistic regression analyses was used to determine the factors associated with placental malaria. The odds ratios were used as a measure of association between independent variables and placental malaria. Socio-demographic variables, malaria preventive practices, and obstetric characteristics were adjusted for cofounding. The respective crude odds ratios (COR) and adjusted odds ratios (AOR) of the variables were determined.

Results

Description of the study participants

The mean age of the participants was 25.34 years (standard deviation [SD] 5.73). The majority of the participants were of primary level or no formal education (61.8%). Nearly all the participants were either unemployed (22%) or self-employed (69%) (Table 1).

Table 1 Socio-demographic characteristics of the participants (n = 366)
Full size table

Obstetric and malaria related characteristics

More than one-half (58.5%) of the women were either primigravidae or secondigravidae (Table 2). Nearly one-half (45.6%) of the participants reported having had malaria infection during pregnancy with nearly one-fifth (19%) of them reporting at least three episodes of malaria infection during pregnancy.

Table 2 Obstetric characteristics of the participants
Full size table

Malaria preventive practices

Close to one-half (44%) of participants who were eligible for IPT-SP reported taking at least three doses of IPT-SP, while 90% of HIV-infected participants were taking co-trimoxazole prophylaxis (Table 3). The majority (80%) of the women had indoor residual spraying protection and used long-lasting insecticidal nets during pregnancy.

Table 3 Malaria prevention practices among study participants
Full size table

Prevalence of placental malaria

The overall prevalence of placental malaria, as determined by RDT, was 4.4% (16/366). The positive RDT result was subjected to microscopy to grade the parasitaemia of the infection. The microscopy smear showed that only 43.7% (7/16) of the positive RDT samples were positive. For the positive microscopy smear, 31.3% (5/16) had mild, 13% (2/16) had moderate parasitaemia. More than half 56.3% (9/16) were negative for the microscopy smear.

Factors associated with placental malaria infection

The age of the woman, marital status, parity, and iron supplementation were associated with placental malaria (Table 4). At multivariable analysis, young age and not receiving iron therapy during pregnancy were associated with placental malaria (Table 5). Women less than 20 years had 3.5 times the odds of having placental malaria as compared to women 20 years and above. Women who did not take antenatal iron-folate drugs had 3.5 times the odds of having placental malaria as compared to women who took iron-folate.

Table 4 Bivariable analysis of the factors associated with placental malaria infection
Full size table
Table 5 Multivariable analysis of factors associated with placenta malaria
Full size table

Discussion

The purpose of this study was to assess the prevalence and the associated factors of placental malaria in Lira District, Northern Uganda. In this study, the prevalence of placental malaria was low (4.4%). The prevalence in the study was lower than the 20% [28], 33% [29], 44.6% [13] and 66.2% [30] in other areas in Uganda. This prevalence was also lower than the average prevalence reported in systematic reviews done in East Africa 27% (16.7–36.4%), Central Africa [31], sub-Saharan Africa 28% [10] and other developing countries 20–30% [32]. The study was conducted during the period of intensive IRS in Northern Uganda. The low prevalence of placental malaria in the study setting could be related to reduced incidence of malaria infection following IRS [33]. Evidence has shown resurgence of malaria infection following discontinuation of IRS [33]. Furthermore, the variation could be attributed to differences in the diagnostics tests, intensity of malaria transmission, the season, characteristics of the participants, and the use of malaria preventive strategies among participants in the different studies. For example, a higher prevalence of 66.2% was reported from a setting with one of the highest malaria transmission [30]. Studies that used placental histology also found higher prevalence rates compared to the RDT used in this study [34]. However, the prevalence in this study was comparable to the 4% in Western Uganda, a low malaria transmission area [35] and 4.6% in a high malaria transmission area in Eastern Uganda [29]. The prevalence of placental malaria in this study was consistent with the range of 0.0–47.1% in a systematic review and meta-analysis of 57 studies conducted in Sub-Saharan Africa [32]. The findings in the study are typical of prevalence found in asymptomatic populations [4]. This implies that placental malaria occurs in asymptomatic patients during pregnancy and, therefore, suggests a need for routine screening of malaria among pregnant women.

In this study, there was insufficient evidence to determine whether first time pregnancies had increased odds of having placental malaria. This could have resulted from the few outcomes of placental malaria positivity, which reduced the power to detect such an association. Other studies have found primigravidae to be more likely to have placental malaria [11, 28]. In this study, placental malaria was found to be higher among women who were less than 20 years of age as compared to women who were 20 years and older. This association was also found by earlier studies [11, 28]. The reduced risk of malaria infection among the older women is plausible since the older women tend to develop immunity from repeated malaria infections [36].

Previous clinical trial studies conducted in children have indicated that iron supplementation in iron-replete non-anaemic children increases the risk of malaria infection [37]. The plausibility of the associated increased odds of acquiring malaria infection has been extended to pregnant women who receive iron supplements during pregnancy [38]. Iron deficiency reduces the risk of peripheral parasitaemia in pregnancy [38]. In this study, however, not taking antenatal iron supplements during pregnancy increased the odds of getting placental malaria. This may be due to the fact that iron supplements are given together with malaria prophylaxis. As such, not taking iron supplements could be a proxy of not taking anti malarials.

There was insufficient evidence to prove that taking atleast three doses of IPT-SP was associated with decreased odds of having placental malaria. Other studies in Uganda have have not found evidence supporting prophylactic IPT-SP to be protective against placental malaria [30, 35]. This could be attributed to the high (93%) parasite resistance to IPT-SP [35, 36].

Limitations of the study

The study had a small proportion of women who had a positive placental malaria finding. The relatively small sample size in this study may have reduced the statistical power of the study to detect the associations between the dependent and independent variables. The inherent limitations of the RDT could have led to under reporting of the prevalence of placental malaria in this study (35). The design of this study limits it from reporting the burden of malaria across seasons. Antenatal cards were used alongside self-reports to collect data for HIV status and malaria preventive practices. Recall bias and social desirability bias may have limited the validity of the study findings.

Conclusion

The prevalence of placental malaria was low in the study. This may be related to low malaria transmissions rates during the period of intensive indoor residual spraying. Placental malaria infection was associated with younger age and not taking iron supplements during pregnancy. Public health measures need to scale up and promote adherence to malaria preventive measures during pregnancy especially among teenage mothers.

Data availability

Data will be made available upon reasonable request.

Abbreviations

ANC:

Antenatal care

AOR:

Adjusted odds ratios

COR:

Crude odds ratios

IPT-SP:

Intermittent preventive treatment of malaria in pregnancy with sulphadoxine pyrimethamine

WHO:

World Health Organization

RDT:

Rapid diagnostic test

HRP2:

Histidine rich protein 2

HIV:

Human immunodeficiency virus

UBOS:

Uganda Bureau of Statistics

UMSI:

Uganda Malaria Indicative Survey

SD:

Standard deviation

References

  1. Uganda National Malaria Control Division (NMCD), Uganda Bureau of Statistics (UBOS), and ICF. 2020. Uganda Malaria Indicator Survey 2018–19. Kampala, Uganda, and Rockville, Maryland, USA.

  2. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Takem EN, D’Alessandro U. Malaria in pregnancy. Mediterr J Hematol Infect Dis. 2013;5: e2013010.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Rogerson SJ, Desai M, Mayor A, Sicuri E, Taylor SM, van Eijk AM. Burden, pathology, and costs of malaria in pregnancy: new developments for an old problem. Lancet Infect Dis. 2018;18:e107–18.

    Article  PubMed  Google Scholar 

  5. De Beaudrap P, Turyakira E, White LJ, Nabasumba C, Tumwebaze B, Muehlenbachs A, et al. Impact of malaria during pregnancy on pregnancy outcomes in a Ugandan prospective cohort with intensive malaria screening and prompt treatment. Malar J. 2013;12:139.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Moore KA, Simpson JA, Scoullar MJ, McGready R, Fowkes FJ. Quantification of the association between malaria in pregnancy and stillbirth: a systematic review and meta-analysis. Lancet Glob Health. 2017;5:e1101–12.

    Article  PubMed  Google Scholar 

  7. Chua CLL, Khoo SKM, Ong JLE, Ramireddi GK, Yeo TW, Teo A. Malaria in pregnancy: from placental infection to its abnormal development and damage. Front Microbiol. 2021;12: 777343.

    Article  PubMed  PubMed Central  Google Scholar 

  8. WHO. World malaria report 2023. Geneva: World Health Organisation; 2023.

    Google Scholar 

  9. WHO. Guidelines for Malaria. Geneva, World Health Organisation, 2023. https://www.who.int/teams/global-malaria-programme. Accessed 17 Feb 2024.

  10. 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.

    Article  PubMed  Google Scholar 

  11. Mpogoro FJ, Matovelo D, Dosani A, Ngallaba S, Mugono M, Mazigo HD. Uptake of intermittent preventive treatment with sulphadoxine-pyrimethamine for malaria during pregnancy and pregnancy outcomes: a cross-sectional study in Geita district, North-Western Tanzania. Malar J. 2014;13:455.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Epstein A, Maiteki-Sebuguzi C, Namuganga JF, Nankabirwa JI, Gonahasa S, Opigo J, et al. Resurgence of malaria in Uganda despite sustained indoor residual spraying and repeated long lasting insecticidal net distributions. PLOS Glob Public Health. 2022;2: e0000676.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Okiring J, Olwoch P, Kakuru A, Okou J, Ochokoru H, Ochieng TA, et al. Household and maternal risk factors for malaria in pregnancy in a highly endemic area of Uganda: a prospective cohort study. Malar J. 2019;18:144.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Briggs J, Ategeka J, Kajubi R, Ochieng T, Kakuru A, Ssemanda C, et al. Impact of microscopic and submicroscopic parasitemia during pregnancy on placental malaria in a high-transmission setting in Uganda. J Infect Dis. 2019;220:457–66.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Mangusho C, Mwebesa E, Izudi J, Aleni M, Dricile R, Ayiasi RM, et al. High prevalence of malaria in pregnancy among women attending antenatal care at a large referral hospital in northwestern Uganda: a cross-sectional study. PLoS ONE. 2023;18: e0283755.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ndeserua R, Juma A, Mosha D, Chilongola J. Risk factors for placental malaria and associated adverse pregnancy outcomes in Rufiji, Tanzania: a hospital based cross sectional study. Afr Health Sci. 2015;15:810–8.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Tukei BB, Beke A, Lamadrid-Figueroa H. Assessing the effect of indoor residual spraying (IRS) on malaria morbidity in Northern Uganda: a before and after study. Malar J. 2017;16:1–9.

    Article  Google Scholar 

  18. Yeka A, Gasasira A, Mpimbaza A, Achan J, Nankabirwa J, Nsobya S, et al. Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop. 2012;121:184–95.

    Article  PubMed  Google Scholar 

  19. Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, et al. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg. 2006;75:219–25.

    Article  PubMed  Google Scholar 

  20. Othoro C, Moore JM, Wannemuehler K, Nahlen BL, Otieno J, Slutsker L, et al. Evaluation of various methods of maternal placental blood collection for immunology studies. Clin Vacc Immunol. 2006;13:568–74.

    Article  CAS  Google Scholar 

  21. Feleke DG, Alemu Y, Yemanebirhane N. Performance of rapid diagnostic tests, microscopy, loop-mediated isothermal amplification (LAMP) and PCR for malaria diagnosis in Ethiopia: a systematic review and meta-analysis. Malar J. 2021;20:1–11.

    Article  Google Scholar 

  22. Kotepui M, Kotepui KU, De Jesus MG, Masangkay FR. Summary of discordant results between rapid diagnosis tests, microscopy, and polymerase chain reaction for detecting Plasmodium mixed infection: a systematic review and meta-analysis. Sci Rep. 2020;10:12765.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fried M, Muehlenbachs A, Duffy PE. Diagnosing malaria in pregnancy: an update. Expert Rev Anti Infect Ther. 2012;10:1177–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gontie GB, Wolde HF, Baraki AG. Prevalence and associated factors of malaria among pregnant women in Sherkole district, Benishangul Gumuz regional state, West Ethiopia. BMC Infect Dis. 2020;20:1–8.

    Article  Google Scholar 

  25. Izuka E, Ugwu E, Obi S, Ozumba B, Nwagha T, Obiora-Izuka C. Prevalence and predictors of placental malaria in human immunodeficiency virus-positive women in Nigeria. Nigerian J Clin Pract. 2017;20:31–6.

    Article  CAS  Google Scholar 

  26. Babalola AS, Idowu OA, Sam-Wobo SO, Fabusoro EJMJ. Risk factors associated with occurrence of placental malaria in a population of parturients in Abeokuta, Ogun State, Nigeria. Malar Wor J. 2015;6.

  27. Bihoun B, Zango SH, Traoré-Coulibaly M, Valea I, Ravinetto R, Van Geertruyden JP, et al. Age-modified factors associated with placental malaria in rural Burkina Faso. BMC Pregnancy Childbirth. 2022;22:1–13.

    Article  Google Scholar 

  28. Namusoke F, Rasti N, Kironde F, Wahlgren M, Mirembe F. Malaria burden in pregnancy at mulago national referral hospital in Kampala, Uganda. Malar Res Treat. 2010;2010: 913857.

    PubMed  PubMed Central  Google Scholar 

  29. Natureeba P, Ades V, Luwedde F, Mwesigwa J, Plenty A, Okong P, et al. Lopinavir/ritonavir-based antiretroviral treatment (ART) versus efavirenz-based ART for the prevention of malaria among HIV-infected pregnant women. J Infect Dis. 2014;210:1938–45.

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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;8:9.

    Article  Google Scholar 

  31. Chico RM, Mayaud P, Ariti C, Mabey D, Ronsmans C, Chandramohan D. Prevalence of malaria and sexually transmitted and reproductive tract infections in pregnancy in sub-Saharan Africa: a systematic review. JAMA. 2012;307:2079–86.

    Article  CAS  PubMed  Google Scholar 

  32. 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:e617–28.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Namuganga JF, Epstein A, Nankabirwa JI, Mpimbaza A, Kiggundu M, Sserwanga A, et al. The impact of stopping and starting indoor residual spraying on malaria burden in Uganda. Nat Commun. 2021;12:2635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kattenberg JH, Ochodo EA, Boer KR, Schallig HD, Mens PF, Leeflang MM. Systematic review and meta-analysis: rapid diagnostic tests versus placental histology, microscopy and PCR for malaria in pregnant women. Malar J. 2011;10:321.

    Article  PubMed  PubMed Central  Google Scholar 

  35. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Tonga C, Kimbi HK, Anchang-Kimbi JK, Nyabeyeu HN, Bissemou ZB, Lehman LG. Malaria risk factors in women on intermittent preventive treatment at delivery and their effects on pregnancy outcome in Sanaga-Maritime, Cameroon. PLoS ONE. 2013;8:6.

    Article  Google Scholar 

  37. Neuberger A, Okebe J, Yahav D, Paul M. Oral iron supplements for children in malaria‐endemic areas. Cochrane Database Syst Rev. 2016;2.

  38. Senga EL, Harper G, Koshy G, Kazembe PN, Brabin BJ. Reduced risk for placental malaria in iron deficient women. Malar J. 2011;10:47.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the valuable input of the research assistants, study participants, the administration of Lira Regional Referral Hospital, and the Nursing Department, Makerere University for their individual contribution in the successful implementation of the study. The project 344 Makerere-SIDA bilateral research programme is acknowledged for funding the study.

Funding

This study was funded by project 344: Makerere-Sweden bilateral research programme (SIDA 344 project under accelerating innovations in reduction of maternal and neonatal mortality in northern Uganda).

Author information

Authors and Affiliations

  1. Department of Nursing, College of Health Sciences, Makerere University, Kampala, Uganda

    Joshua Epuitai, Rose Chalo Nabirye & Lydia Kabiri

  2. Department of Nursing, Faculty of Health Sciences, Busitema University, Mbale, Uganda

    Joshua Epuitai

  3. Department of Pediatrics, College of Health Sciences, Makerere University, Kampala, Uganda

    Grace Ndeezi & James K. Tumwine

  4. Department of Community and Public Health, Faculty of Health Sciences, Busitema University, Mbale, Uganda

    David Mukunya & Faith Oguttu

  5. Department of Research, Nikao Medical Center, Kampala, Uganda

    David Mukunya

  6. Department of Epidemiology and Biostatistics, School of Public Health, Makerere University, Kampala, Uganda

    Josephine Tumuhamye

  7. Department of Pediatrics, Faculty of Health Sciences, Kabale University, Kabale, Uganda

    James K. Tumwine

Authors
  1. Joshua Epuitai
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Grace Ndeezi
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Rose Chalo Nabirye
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Lydia Kabiri
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. David Mukunya
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Josephine Tumuhamye
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Faith Oguttu
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. James K. Tumwine
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

JE, JKT and GN were involved in the conceptualization of the study. JE designed the study, collected and analyzed the data, and drafted the manuscript. DM, JT, FO were involved in reviewing the manuscript. CRN and LK provided the overall oversight in the design and implementation of the study. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Joshua Epuitai.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was obtained from the Makerere University, School of Health Science Ethics and Research Committee (reference number: 2018-049). Permission to conduct the study in the hospital was obtained from the hospital administration. Written informed consent was obtained from the potential study participants who were in their first stage of labor. The researchers addressed cultural values regarding placental handling. Participants were informed of the test results and those with positive test results were linked to care in the hospital.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Epuitai, J., Ndeezi, G., Nabirye, R.C. et al. Prevalence and factors associated with placental malaria in Lira District, Northern Uganda: a cross-sectional study. Malar J 23, 360 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12936-024-05187-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12936-024-05187-4

Keywords

Malaria Journal

ISSN: 1475-2875

Contact us