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High burden of asymptomatic malaria and anaemia despite high adherence to malaria control measures: a cross-sectional study among pregnant women across two seasons in a malaria-endemic setting in Ghana

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Abstract

Purpose

Anaemia remains a serious concern among pregnant women, and thus, it is closely monitored from the onset of pregnancy through to delivery to help prevent adverse maternal and neonatal outcomes. In malaria-endemic settings, continuous low-level carriage of P. falciparum parasites is common and its contribution to maternal anaemia should not be underestimated. In this study, we evaluated the impact of adherence to malaria control measures [number of antenatal clinics (ANC) attended, supervised intake of sulphadoxine pyrimethamine (SP), and use of insecticide treated bed nets (ITNs)] on asymptomatic malaria and anaemia outcomes among pregnant women on ANC in hospitals in the Central region of Ghana.

Methods

The study was conducted during two seasons; October–November 2020 (dry season, n = 124) and May–June 2021 (rainy season, n = 145). Among the women, there was a high adherence to the control measures for both seasons (ANC ≥ 3 visits; ~ 82.0%, intake of SP; ~ 80.0% and ITNs use; ~ 75.0%).

Results

Asymptomatic P. falciparum carriage was high for both seasons (44.4% for the dry season; 46.9% for the rainy season). Correspondingly, the occurrence of anaemia was high for both seasons (57.3% for the dry season; 68.3% for the rainy season) and was strongly predicted by carriage of P. falciparum parasites. Despite the high adherence to ANC protocols, asymptomatic P. falciparum infection was common and contributed to the high burden of maternal anaemia.

Conclusions

Our findings emphasize the need for improved control measures that can clear asymptomatic/sub-microscopic P. falciparum infection and protect against malaria-induced anaemia among pregnant women attending ANC in malaria endemic-settings.

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Data availability

Data supporting the findings of this work are captured here. Raw data can be made available upon reasonable request.

References

  1. World Health Organization. World malaria report 2021. Geneva: World Health Organization; 2021. p. 42–3. Licence: CC BY-NC-SA 3.0 IGO.

  2. Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, Joshi H. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:1–15.

    Article  Google Scholar 

  3. Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7:105–17.

    Article  CAS  PubMed  Google Scholar 

  4. Yimam Y, Nateghpour M, Mohebali M, Abbaszadeh Afshar MJ. A systematic review and meta-analysis of asymptomatic malaria infection in pregnant women in Sub-Saharan Africa: a challenge for malaria elimination efforts. PLoS One. 2021;16: e0248245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Menendez C, Ordi J, Ismail M, Ventura P, Aponte J, Kahigwa E, Font F, Alonso P. The impact of placental malaria on gestational age and birth weight. J Infect Dis. 2000;181:1740–5.

    Article  CAS  PubMed  Google Scholar 

  6. Steketee RW, Nahlen BL, Parise ME, Menendez C. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg. 2001;64:28–35.

    Article  CAS  PubMed  Google Scholar 

  7. Van Geertruyden J-P, Thomas F, Erhart A, D’Alessandro U. The contribution of malaria in pregnancy to perinatal mortality. Am J Trop Med Hyg. 2004;71:35–40.

    Article  PubMed  Google Scholar 

  8. McLean E, Cogswell M, Egli I, Wojdyla D, De Benoist B. Worldwide prevalence of anaemia, WHO vitamin and mineral nutrition information system, 1993–2005. Public Health Nutr. 2009;12:444–54.

    Article  PubMed  Google Scholar 

  9. Grum T, Brhane E, Hintsa S, Kahsay G. Magnitude and factors associated with anemia among pregnant women attending antenatal care in public health centers in central zone of Tigray region, northern Ethiopia: a cross sectional study. BMC Pregnancy Childbirth. 2018;18:1–7.

    Article  Google Scholar 

  10. Adam I, ALhabardi NA, Al-Wutayd O, Khamis A. Prevalence of schistosomiasis and its association with anemia among pregnant women: a systematic review and meta-analysis. Parasites Vectors. 2021;14:1–10.

    Article  Google Scholar 

  11. Correa-Agudelo E, Kim H-Y, Musuka GN, Mukandavire Z, Miller FD, Tanser F, Cuadros DF. The epidemiological landscape of anemia in women of reproductive age in sub-Saharan Africa. Sci Rep. 2021;11:1–10.

    Article  Google Scholar 

  12. Matangila JR, Lufuluabo J, Ibalanky AL, Inocêncio da Luz RA, Lutumba P, Van Geertruyden J-P. Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo. Malar J. 2014;13:1–10.

    Article  Google Scholar 

  13. Tamura T, Picciano MF. Folate and human reproduction. Am J Clin Nutr. 2006;83:993–1016.

    Article  CAS  PubMed  Google Scholar 

  14. Stephen G, Mgongo M, Hussein Hashim T, Katanga J, Stray-Pedersen B, Msuya SE. Anaemia in pregnancy: prevalence, risk factors, and adverse perinatal outcomes in Northern Tanzania. Anemia. 2018;2018: 1846280.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Debella A, Eyeberu A, Getachew T, Atnafe G, Geda B, Dheresa M. Perinatal outcomes in anemic pregnant women in public hospitals of eastern Ethiopia. Int Health. 2022;15:274–80.

    Article  PubMed Central  Google Scholar 

  16. Kidanto HL, Mogren I, Lindmark G, Massawe S, Nystrom L. Risks for preterm delivery and low birth weight are independently increased by severity of maternal anaemia. S Afr Med J. 2009;99:98–102.

    CAS  PubMed  Google Scholar 

  17. Mehrotra M, Yadav S, Deshpande A, Mehrotra H. A study of the prevalence of anemia and associated sociodemographic factors in pregnant women in Port Blair, Andaman and Nicobar Islands. J Fam Med Prim Care. 2018;7:1288.

    Article  Google Scholar 

  18. Nyamtema AS, Jong AB-D, Urassa DP, Hagen JP, van Roosmalen J. The quality of antenatal care in rural Tanzania: what is behind the number of visits? BMC Pregnancy Childbirth. 2012;12:1–5.

    Article  Google Scholar 

  19. World Health Organization. WHO recommendations on antenatal care for a positive pregnancy experience: summary: highlights and key messages from the World Health Organization’s 2016 global recommendations for routine antenatal care. Geneva: World Health Organization; 2018.

    Google Scholar 

  20. Mosha D, Chilongola J, Ndeserua R, Mwingira F, Genton B. Effectiveness of intermittent preventive treatment with sulfadoxine–pyrimethamine during pregnancy on placental malaria, maternal anaemia and birthweight in areas with high and low malaria transmission intensity in T anzania. Trop Med Int Health. 2014;19:1048–56.

    Article  PubMed  Google Scholar 

  21. Mikomangwa WP, Oms M, Aklillu E, Kamuhabwa AA. Adverse birth outcomes among mothers who received intermittent preventive treatment with Sulphadoxine-Pyrimethamine in the low malaria transmission region. BMC Pregnancy Childbirth. 2019;19:1–11.

    Article  CAS  Google Scholar 

  22. Agyeman YN, Newton S, Annor RB, Owusu-Dabo E. Intermittent preventive treatment comparing two versus three doses of sulphadoxine pyrimethamine (IPTp-SP) in the prevention of anaemia in pregnancy in Ghana: a cross-sectional study. PLoS One. 2021;16: e0250350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. COSMIC Consortium. Community-based malaria screening and treatment for pregnant women receiving standard intermittent preventive treatment with sulfadoxine-pyrimethamine: a multicenter (The Gambia, Burkina Faso, and Benin) cluster-randomized controlled trial. Clin Infect Dis. 2019;68:586–96.

    Article  Google Scholar 

  24. Kayentao K, Garner P, van Eijk AM, Naidoo I, Roper C, Mulokozi A, MacArthur JR, Luntamo M, Ashorn P, Doumbo OK. Intermittent preventive therapy for malaria during pregnancy using 2 vs 3 or more doses of sulfadoxine-pyrimethamine and risk of low birth weight in Africa: systematic review and meta-analysis. JAMA. 2013;309:594–604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Berry I, Walker P, Tagbor H, Bojang K, Coulibaly SO, Kayentao K, Williams J, Oduro A, Milligan P, Chandramohan D. Seasonal dynamics of malaria in pregnancy in West Africa: evidence for carriage of infections acquired before pregnancy until first contact with antenatal care. Am J Trop Med Hyg. 2018;98:534.

    Article  PubMed  Google Scholar 

  26. Ofori MF, Lamptey H, Dickson EK, Kyei-Baafour E, Hviid L. Etiology of placental Plasmodium falciparum malaria in African women. J Infect Dis. 2018;218:277–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Desai M, Gutman J, Taylor SM, Wiegand RE, Khairallah C, Kayentao K, Ouma P, Coulibaly SO, Kalilani L, Mace KE. Impact of sulfadoxine-pyrimethamine resistance on effectiveness of intermittent preventive therapy for malaria in pregnancy at clearing infections and preventing low birth weight. Clin Infect Dis. 2016;62:323–33.

    Article  CAS  PubMed  Google Scholar 

  28. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization; 2011.

    Google Scholar 

  29. Anabire NG, Aryee PA, Abdul-Karim A, Abdulai IB, Quaye O, Awandare GA, Helegbe GK. Prevalence of malaria and hepatitis B among pregnant women in Northern Ghana: comparing RDTs with PCR. PLoS One. 2019;14: e0210365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ampofo GD, Tagbor H, Bates I. Effectiveness of pregnant women’s active participation in their antenatal care for the control of malaria and anaemia in pregnancy in Ghana: a cluster randomized controlled trial. Malar J. 2018;17:1–15.

    Article  Google Scholar 

  31. Severe Malaria Observatory. Knowledge sharing for severe malaria, Ghana; Malaria prevention; 2020. https://www.severemalaria.org/countries/ghana#&gid=4&pid=1%0A. Cited 31 Oct 2022.

  32. Dun-Dery F, Kuunibe N, Meissner P, Winkler V, Jahn A, Müller O. Determinants of the use of insecticide-treated mosquito nets in pregnant women: a mixed-methods study in Ghana. Int Health. 2022;14:619–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Awine T, Malm K, Bart-Plange C, Silal SP. Towards malaria control and elimination in Ghana: challenges and decision making tools to guide planning. Glob Health Action. 2017;10: 1381471.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Nwaefuna EK, Afoakwah R, Orish VN, Egyir-Yawson A, Boampong J. Effectiveness of intermittent preventive treatment in pregnancy with sulphadoxine-pyrimethamine against submicroscopic falciparum malaria in central region, Ghana. J Parasitol Res. 2015;2015: 959427.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rouamba T, Samadoulougou S, Ouédraogo M, Hien H, Tinto H, Kirakoya-Samadoulougou F. Asymptomatic malaria and anaemia among pregnant women during high and low malaria transmission seasons in Burkina Faso: household-based cross-sectional surveys in Burkina Faso, 2013 and 2017. Malar J. 2021;20:1–13.

    Article  Google Scholar 

  36. Thompson JM, Eick SM, Dailey C, Dale AP, Mehta M, Nair A, Cordero JF, Welton M. Relationship between pregnancy-associated malaria and adverse pregnancy outcomes: a systematic review and meta-analysis. J Trop Pediatr. 2020;66:327–38.

    Article  PubMed  Google Scholar 

  37. Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–39.

    Article  CAS  PubMed  Google Scholar 

  38. Galatas B, Bassat Q, Mayor A. Malaria parasites in the asymptomatic: looking for the hay in the haystack. Trends Parasitol. 2016;32:296–308.

    Article  PubMed  Google Scholar 

  39. Orish VN, Onyeabor OS, Boampong JN, Afoakwah R, Nwaefuna E, Acquah S, Sanyaolu AO, Iriemenam NC. Prevalence of intermittent preventive treatment with sulphadoxine-pyrimethamine (IPTp-SP) use during pregnancy and other associated factors in Sekondi-Takoradi, Ghana. Afr Health Sci. 2015;15:1087–96.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Desai M, Ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7:93–104.

    Article  PubMed  Google Scholar 

  41. Homann MV, Emami SN, Yman V, Stenström C, Sondén K, Ramström H, Karlsson M, Asghar M, Färnert A. Detection of malaria parasites after treatment in travelers: a 12-months longitudinal study and statistical modelling analysis. EBioMedicine. 2017;25:66–72.

    Article  Google Scholar 

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Acknowledgements

The research was supported by DANIDA (grant MAVARECA-II; 17-02-KU). The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agency. NGA was supported by a MAVARECA-II PhD studentship. We thank all the study participants and the numerous midwives, medical doctors, physician assistants, medical laboratory scientist and nurses in the various health facilities (Abura Dunkwa District Hospital, Moree Health Centre, Effutu Health Centre, Cape Coast and Mercy Women’s Catholic Hospital, Mankessim) for their enormous support. Special thank you to the Department of Immunology, Noguchi Memorial Institute for Medical research field team members including Rev. Alex Danso-Coffie and Sophia Ampaw for supporting in participant recruitment and enrolment.

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Authors and Affiliations

  1. West African Centre for Cell Biology of Infectious Pathogens, Department of Biochemistry, Cell and Molecular Biology, University of Ghana, Accra, Ghana

    Nsoh Godwin Anabire, Gordon A. Awandare & Michael F. Ofori

  2. Department of Immunology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, Ghana

    Nsoh Godwin Anabire, Belinda Aculley, Abigail Pobee, Eric Kyei-Baafour & Michael F. Ofori

  3. Department of Biochemistry and Molecular Medicine, School of Medicine, University for Development Studies, Tamale, Ghana

    Nsoh Godwin Anabire

  4. Centre for Medical Parasitology, Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Nsoh Godwin Anabire, Maria del Pilar Quintana & Lars Hviid

  5. Department of Infectious Diseases, Rigshospitalet, Copenhagen, Denmark

    Lars Hviid

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  1. Nsoh Godwin Anabire
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Contributions

MO and NGA conceived the idea, and designed the study together with LH, MdPQ and GAA. NGA, BA, AP and EKB conducted data collection and data curation. NGA conducted data analysis and interpretation of findings, and wrote the first draft manuscript. MO, LH, MdPQ and GAA critically reviewed the manuscript. All authors read, improved and approved the final manuscript. LH and MO secured the funding and supervised the study.

Corresponding author

Correspondence to Michael F. Ofori.

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Anabire, N.G., Aculley, B., Pobee, A. et al. High burden of asymptomatic malaria and anaemia despite high adherence to malaria control measures: a cross-sectional study among pregnant women across two seasons in a malaria-endemic setting in Ghana. Infection 51, 1717–1729 (2023). https://doi.org/10.1007/s15010-023-02058-z

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