Skip to main content
Top
Published in:

Open Access 01-12-2023 | Malaria | Research

Increased peripartum mortality associated with maternal subclinical malaria in Mozambique

Authors: Nieves Jaén-Sánchez, Gloria González-Azpeitia, Cristina Carranza-Rodriguez, Nicholas Manwere, Paloma Garay-Sánchez, Laura Vallejo-Torres, José-Luis Pérez-Arellano

Published in: Malaria Journal | Issue 1/2023

Login to get access

Abstract

Background

Plasmodium falciparum infection in pregnant women in sub-Saharan Africa is often asymptomatic. As these forms of malaria are often submicroscopic and difficult to diagnose by conventional methods (microscopy and/or rapid diagnostic test), diagnosis requires the use of molecular techniques such as polymerase chain reaction (PCR). This study analyses the prevalence of subclinical malaria and its association with adverse maternal and neonatal outcomes, a topic that has been scarcely evaluated in the literature.

Methods

A cross-sectional study was conducted using semi-nested multiplex PCR to assess the presence of P. falciparum in placental and peripheral blood of 232 parturient pregnant women at the Hospital Provincial de Tete, Mozambique between March 2017 and May 2019. Multivariate regressions were performed to assess the associations of maternal subclinical malaria with several maternal and neonatal outcomes after controlling for the presence of preeclampsia/eclampsia (PE/E) and HIV infection, as well as for other maternal and pregnancy characteristics.

Results

In total, 17.2% (n = 40) of the women studied had positive PCR for P. falciparum (7 in placental blood only, 3 in peripheral blood only). We found a significant association between subclinical malaria and a higher peripartum mortality risk, which persisted after controlling for maternal comorbidity and maternal and pregnancy characteristics (adjusted odds ratio: 3.50 [1.11–10.97]). In addition, PE/E and HIV infections were also significantly associated with several adverse maternal and neonatal outcomes.

Conclusion

This study demonstrated the association of subclinical malaria, as well as of PE/E and HIV, in pregnant women with adverse maternal and neonatal outcomes. Therefore, molecular methods may be sensitive tools to identify asymptomatic infections that can reduce the impact on peripartum mortality and their contribution to sustained transmission of the parasite in endemic countries.
Literature
1.
go back to reference WHO. World malaria report 2021. Geneva: World Health Organization; 2021. WHO. World malaria report 2021. Geneva: World Health Organization; 2021.
2.
go back to reference Tilahun A, Yimer M, Gelaye W, Tegegne B. Prevalence of asymptomatic Plasmodium species infection and associated factors among pregnant women attending antenatal care at Fendeka town health facilities, Jawi District, North West Ethiopia: a cross-sectional study. PLoS ONE. 2020;154:e0231477.CrossRef Tilahun A, Yimer M, Gelaye W, Tegegne B. Prevalence of asymptomatic Plasmodium species infection and associated factors among pregnant women attending antenatal care at Fendeka town health facilities, Jawi District, North West Ethiopia: a cross-sectional study. PLoS ONE. 2020;154:e0231477.CrossRef
3.
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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference Hounkonnou CPA, Briand V, Fievet N, Accrombessi M, Yovo E, Mama A, et al. Dynamics of submicroscopic Plasmodium falciparum infections throughout pregnancy: a preconception cohort study in Benin. Clin Infect Dis. 2020;71:166–74.CrossRefPubMed Hounkonnou CPA, Briand V, Fievet N, Accrombessi M, Yovo E, Mama A, et al. Dynamics of submicroscopic Plasmodium falciparum infections throughout pregnancy: a preconception cohort study in Benin. Clin Infect Dis. 2020;71:166–74.CrossRefPubMed
5.
6.
go back to reference Boene H, Vidler M, Augusto O, Sidat M, Macete E, Menéndez C, et al. CLIP feasibility working group. Community health worker knowledge and management of pre-eclampsia in southern Mozambique. Reprod Health. 2016;13(Suppl 2):105.CrossRefPubMedPubMedCentral Boene H, Vidler M, Augusto O, Sidat M, Macete E, Menéndez C, et al. CLIP feasibility working group. Community health worker knowledge and management of pre-eclampsia in southern Mozambique. Reprod Health. 2016;13(Suppl 2):105.CrossRefPubMedPubMedCentral
7.
go back to reference Sacoor C, Payne B, Augusto O, Vilanculo F, Nhacolo A, Vidler M, et al. CLIP feasibility working group Health and socio-demographic profile of women of reproductive age in rural communities of southern Mozambique. PLoS ONE. 2018;13:e0184249.CrossRefPubMedPubMedCentral Sacoor C, Payne B, Augusto O, Vilanculo F, Nhacolo A, Vidler M, et al. CLIP feasibility working group Health and socio-demographic profile of women of reproductive age in rural communities of southern Mozambique. PLoS ONE. 2018;13:e0184249.CrossRefPubMedPubMedCentral
8.
go back to reference Menéndez C, Romagosa C, Ismail MR, Carrilho C, Saute F, Osman N, et al. An autopsy study of maternal mortality in Mozambique: the contribution of Infectious Diseases. PLoS Med. 2008;5:e44.CrossRefPubMedPubMedCentral Menéndez C, Romagosa C, Ismail MR, Carrilho C, Saute F, Osman N, et al. An autopsy study of maternal mortality in Mozambique: the contribution of Infectious Diseases. PLoS Med. 2008;5:e44.CrossRefPubMedPubMedCentral
9.
go back to reference Obiri D, Erskine IJ, Oduro D, Kusi KA, Amponsah J, Gyan BA, et al. Histopathological lesions and exposure to Plasmodium falciparum infections in the placenta increases the risk of preeclampsia among pregnant women. Sci Rep. 2020;10:8280.CrossRefPubMedPubMedCentral Obiri D, Erskine IJ, Oduro D, Kusi KA, Amponsah J, Gyan BA, et al. Histopathological lesions and exposure to Plasmodium falciparum infections in the placenta increases the risk of preeclampsia among pregnant women. Sci Rep. 2020;10:8280.CrossRefPubMedPubMedCentral
10.
go back to reference Boyajian T, Shah PS, Murphy KE. Risk of preeclampsia in HIV-positive pregnant women receiving HAART: a matched cohort study. J Obstet Gynaecol Can. 2012;34:136–41.CrossRefPubMed Boyajian T, Shah PS, Murphy KE. Risk of preeclampsia in HIV-positive pregnant women receiving HAART: a matched cohort study. J Obstet Gynaecol Can. 2012;34:136–41.CrossRefPubMed
11.
go back to reference Mahamar A, Andemel N, Swihart B, Sidibe Y, Gaoussou S, Barry A, et al. Malaria infection is common and associated with perinatal mortality and preterm delivery despite widespread use of chemoprevention in Mali: an observational study 2010 to 2014. Clin Infect Dis. 2021;73:1355–61.CrossRefPubMedPubMedCentral Mahamar A, Andemel N, Swihart B, Sidibe Y, Gaoussou S, Barry A, et al. Malaria infection is common and associated with perinatal mortality and preterm delivery despite widespread use of chemoprevention in Mali: an observational study 2010 to 2014. Clin Infect Dis. 2021;73:1355–61.CrossRefPubMedPubMedCentral
12.
go back to reference Ategeka J, Kakuru A, Kajubi R, Wasswa R, Ochokoru H, Arinaitwe E, et al. Relationships between measures of malaria at delivery and adverse birth outcomes in a high-transmission area of Uganda. J Infect Dis. 2020;222:863–70.CrossRefPubMedPubMedCentral Ategeka J, Kakuru A, Kajubi R, Wasswa R, Ochokoru H, Arinaitwe E, et al. Relationships between measures of malaria at delivery and adverse birth outcomes in a high-transmission area of Uganda. J Infect Dis. 2020;222:863–70.CrossRefPubMedPubMedCentral
13.
go back to reference Gaoussou S, Attaher O, Swihart B, Traore M, Diarra S, Soumbounou IH, et al. Pregnancy outcomes in a malaria-exposed Malian cohort of women of child-bearing age. Front Med (Lausanne). 2022;9:1061538.CrossRefPubMed Gaoussou S, Attaher O, Swihart B, Traore M, Diarra S, Soumbounou IH, et al. Pregnancy outcomes in a malaria-exposed Malian cohort of women of child-bearing age. Front Med (Lausanne). 2022;9:1061538.CrossRefPubMed
15.
go back to reference 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 Vaccine Immunol. 2006;13:568–74.CrossRefPubMedPubMedCentral 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 Vaccine Immunol. 2006;13:568–74.CrossRefPubMedPubMedCentral
16.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.CrossRefPubMed Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.CrossRefPubMed
18.
go back to reference von Dadelszen P, Magee LA. Pre-eclampsia: an update. Curr Hypertens Rep. 2014;16:454.CrossRef von Dadelszen P, Magee LA. Pre-eclampsia: an update. Curr Hypertens Rep. 2014;16:454.CrossRef
19.
go back to reference Mol BWJ, Roberts CT, Thangaratinam S, Magee LA, de Groot CJM, Hofmeyr GJ. Pre-eclampsia. Lancet. 2016;387:999–1011.CrossRefPubMed Mol BWJ, Roberts CT, Thangaratinam S, Magee LA, de Groot CJM, Hofmeyr GJ. Pre-eclampsia. Lancet. 2016;387:999–1011.CrossRefPubMed
20.
go back to reference Academy A, of Pediatrics Committee on Fetus and Newborn. American college of obstetricians and gynecologists committee on obstetric practice. Apgar Score Pediatrics. 2015;136:819–22. Academy A, of Pediatrics Committee on Fetus and Newborn. American college of obstetricians and gynecologists committee on obstetric practice. Apgar Score Pediatrics. 2015;136:819–22.
21.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
22.
go back to reference Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009;200:1509–17.CrossRefPubMed Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009;200:1509–17.CrossRefPubMed
23.
go back to reference Ntoumi F, Bakoua D, Fesse A, Komboa M, Vouvoungui JC, Koukouikila-Koussounda F. Characterization of asymptomatic Plasmodium falciparum infection and its risk factors in pregnant women from the Republic of Congo. Acta Trop. 2016;153:111–5.CrossRef Ntoumi F, Bakoua D, Fesse A, Komboa M, Vouvoungui JC, Koukouikila-Koussounda F. Characterization of asymptomatic Plasmodium falciparum infection and its risk factors in pregnant women from the Republic of Congo. Acta Trop. 2016;153:111–5.CrossRef
24.
25.
go back to reference Roux AT, Maharaj L, Oyegoke O, Akoniyon OP, Adeleke MA, Maharaj R, et al. Chloroquine and sulfadoxine-pyrimethamine resistance in sub-Saharan Africa—a review. Front Genet. 2021;12:668574.CrossRefPubMedPubMedCentral Roux AT, Maharaj L, Oyegoke O, Akoniyon OP, Adeleke MA, Maharaj R, et al. Chloroquine and sulfadoxine-pyrimethamine resistance in sub-Saharan Africa—a review. Front Genet. 2021;12:668574.CrossRefPubMedPubMedCentral
27.
go back to reference WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015. WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015.
28.
go back to reference Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal–fetal conflict during placental malaria. PLoS Med. 2006;3:e446.CrossRefPubMedPubMedCentral Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal–fetal conflict during placental malaria. PLoS Med. 2006;3:e446.CrossRefPubMedPubMedCentral
29.
go back to reference Ndao CT, Dumont A, Fievet N, Doucoure S, Gaye A, Lehesran JY. Placental malarial infection as a risk factor for hypertensive disorders during pregnancy in Africa: a case-control study in an urban area of Senegal. West Africa Am J Epidemiol. 2009;170:847–53.CrossRefPubMed Ndao CT, Dumont A, Fievet N, Doucoure S, Gaye A, Lehesran JY. Placental malarial infection as a risk factor for hypertensive disorders during pregnancy in Africa: a case-control study in an urban area of Senegal. West Africa Am J Epidemiol. 2009;170:847–53.CrossRefPubMed
30.
go back to reference Adam I, Elhassan EM, Mohmmed AA, Salih MM, Elbashir MI. Malaria and pre-eclampsia in an area with unstable malaria transmission in Central Sudan. Malar J. 2011;10:258.CrossRefPubMedPubMedCentral Adam I, Elhassan EM, Mohmmed AA, Salih MM, Elbashir MI. Malaria and pre-eclampsia in an area with unstable malaria transmission in Central Sudan. Malar J. 2011;10:258.CrossRefPubMedPubMedCentral
31.
go back to reference Etard JF, Kodio B, Ronsmans C. Seasonal variation in direct obstetric mortality in rural Senegal: Role of malaria? Am J Trop Med Hyg. 2003;68:503–4.CrossRefPubMed Etard JF, Kodio B, Ronsmans C. Seasonal variation in direct obstetric mortality in rural Senegal: Role of malaria? Am J Trop Med Hyg. 2003;68:503–4.CrossRefPubMed
32.
go back to reference Dosoo DK, Chandramohan D, Atibilla D, Oppong FB, Ankrah L, Kayan K, et al. Epidemiology of malaria among pregnant women during their first antenatal clinic visit in the middle belt of Ghana: a cross sectional study. Malar J. 2020;19:381.CrossRefPubMedPubMedCentral Dosoo DK, Chandramohan D, Atibilla D, Oppong FB, Ankrah L, Kayan K, et al. Epidemiology of malaria among pregnant women during their first antenatal clinic visit in the middle belt of Ghana: a cross sectional study. Malar J. 2020;19:381.CrossRefPubMedPubMedCentral
33.
go back to reference Mlugu EM, Minzi O, Kamuhabwa A, Aklillu E. Prevalence and correlates of asymptomatic malaria and anemia on first antenatal care visit among pregnant women in Southeast, Tanzania. Int J Environ Res Public Health. 2020;17:3123.CrossRefPubMedPubMedCentral Mlugu EM, Minzi O, Kamuhabwa A, Aklillu E. Prevalence and correlates of asymptomatic malaria and anemia on first antenatal care visit among pregnant women in Southeast, Tanzania. Int J Environ Res Public Health. 2020;17:3123.CrossRefPubMedPubMedCentral
34.
go back to reference Ndwiga C, Odwe G, Pooja S, Ogutu O, Osoti A, Warren CE. Clinical presentation and outcomes of pre-eclampsia and eclampsia at a national hospital, Kenya: a retrospective cohort study. PLoS ONE. 2020;15:e0233323.CrossRefPubMedPubMedCentral Ndwiga C, Odwe G, Pooja S, Ogutu O, Osoti A, Warren CE. Clinical presentation and outcomes of pre-eclampsia and eclampsia at a national hospital, Kenya: a retrospective cohort study. PLoS ONE. 2020;15:e0233323.CrossRefPubMedPubMedCentral
35.
go back to reference Omotayo M, Dickin K, Stolzfus R. Perinatal mortality due to pre-eclampsia in Africa: a comprehensive and integrated approach is needed. Glob Health Sci Pract. 2016;4:350–1.CrossRefPubMedPubMedCentral Omotayo M, Dickin K, Stolzfus R. Perinatal mortality due to pre-eclampsia in Africa: a comprehensive and integrated approach is needed. Glob Health Sci Pract. 2016;4:350–1.CrossRefPubMedPubMedCentral
36.
go back to reference Calvert C, Ronsmans C. HIV and the risk of direct obstetric complications: a systematic review and meta-analysis. PLoS ONE. 2013;4:e74848.CrossRef Calvert C, Ronsmans C. HIV and the risk of direct obstetric complications: a systematic review and meta-analysis. PLoS ONE. 2013;4:e74848.CrossRef
37.
go back to reference Gonzalez R, Rupérez M, Sevene E, Vala A, Maculuve S, Bulo H, et al. Effects of HIV infection on maternal and neonatal health in southern Mozambique: a prospective cohort study. PLoS ONE. 2017;12:e0178134.CrossRefPubMedPubMedCentral Gonzalez R, Rupérez M, Sevene E, Vala A, Maculuve S, Bulo H, et al. Effects of HIV infection on maternal and neonatal health in southern Mozambique: a prospective cohort study. PLoS ONE. 2017;12:e0178134.CrossRefPubMedPubMedCentral
Metadata
Title
Increased peripartum mortality associated with maternal subclinical malaria in Mozambique
Authors
Nieves Jaén-Sánchez
Gloria González-Azpeitia
Cristina Carranza-Rodriguez
Nicholas Manwere
Paloma Garay-Sánchez
Laura Vallejo-Torres
José-Luis Pérez-Arellano
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2023
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-023-04613-3

Other articles of this Issue 1/2023

Malaria Journal 1/2023 Go to the issue

A quick guide to ECGs

Improve your ECG interpretation skills with this comprehensive, rapid, interactive course. Expert advice provides detailed feedback as you work through 50 ECGs covering the most common cardiac presentations to ensure your practice stays up to date. 

PD Dr. Carsten W. Israel
Developed by: Springer Medizin
Start the cases

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
Read more