Available online on 15.07.2024 at ijmspr.com

International Journal of Medical Sciences and Pharma Research

Open Access to Medical Science and Pharma Research

Copyright  © 2024 The  Author(s): This is an open-access article distributed under the terms of the CC BY-NC 4.0 which permits unrestricted use, distribution, and reproduction in any medium for non-commercial use provided the original author and source are credited

Maternal Malaria and the Risk of Subsequent Pregnancy Complications

^*Emmanuel Ifeanyi Obeagu ¹ and Getrude Uzoma Obeagu ²

¹ Department of Medical Laboratory Science, Kampala International University, Ishaka, Uganda.

² School of Nursing Science, Kampala International University, Ishaka, Uganda.

 

 

Introduction

Maternal malaria, predominantly caused by the protozoan parasite Plasmodium falciparum, remains a significant public health concern in many tropical and subtropical regions. This disease poses severe risks to both maternal and fetal health, leading to complications such as anemia, preterm birth, and low birth weight. Maternal malaria occurs when the parasite infects and sequesters in the placenta, causing local inflammation and impairing placental function. While the immediate effects of malaria during pregnancy are well-documented, there is growing recognition of its potential long-term impacts on subsequent pregnancies.^1-2 During an acute malaria infection, the placenta becomes a site of intense inflammatory response due to the accumulation of infected erythrocytes. This inflammation can lead to placental damage, disrupting the exchange of nutrients and oxygen between mother and fetus. Complications such as severe maternal anemia, preterm birth, and intrauterine growth restriction are commonly observed. The immediate health consequences for both mother and baby highlight the critical need for effective malaria management during pregnancy.^3-5 The damage inflicted on the placenta during an episode of malaria is not always fully resolved after the infection is treated. Chronic placental damage, including scarring and impaired function, can persist long after the initial infection. This residual damage can have lasting implications for future pregnancies. The compromised placental environment may lead to recurrent issues in subsequent pregnancies, such as increased risks of preterm delivery or low birth weight, underscoring the need to understand how previous malaria infections influence future reproductive health.^6-8 Maternal malaria can induce long-lasting changes in the maternal immune system. The immune dysregulation observed during an acute malaria episode may persist, potentially affecting future pregnancies. Altered cytokine profiles, increased levels of pro-inflammatory mediators, and changes in immune cell function can impact pregnancy outcomes. These immune alterations may contribute to an increased risk of complications in subsequent pregnancies by affecting placental function and maternal immune responses.^9-10

Chronic inflammation resulting from previous malaria infections may have a significant impact on future pregnancies. Persistent inflammatory responses can lead to a pro-inflammatory environment that may increase the risk of complications such as preterm labor, placental abruption, or other adverse outcomes. Understanding the role of chronic inflammation in influencing subsequent pregnancy complications is essential for developing strategies to mitigate these risks.^11-12 The effects of maternal malaria on fetal health can extend beyond the immediate pregnancy. Infants born to mothers with a history of malaria may be at higher risk for developmental issues and health complications later in life. The potential for long-term health effects on the child, such as impaired growth or developmental delays, highlights the importance of addressing maternal malaria comprehensively to protect both maternal and fetal health across multiple pregnancies.^13-14 The potential long-term effects of maternal malaria on subsequent pregnancies have significant public health implications. These effects underscore the need for comprehensive malaria prevention and treatment strategies that consider not only the immediate impacts but also the long-term consequences for reproductive health. Effective management of maternal malaria, including prevention, early diagnosis, and treatment, is crucial for improving maternal and fetal health outcomes and reducing the burden of malaria in affected regions.^15-16

Maternal Malaria and Immediate Pregnancy Outcomes

Maternal malaria, predominantly caused by Plasmodium falciparum, poses serious risks to both maternal and fetal health. The disease's effects on pregnancy outcomes are well-documented, with immediate complications including severe anemia, preterm birth, and low birth weight. This section explores how maternal malaria impacts immediate pregnancy outcomes, focusing on the mechanisms by which the infection disrupts normal pregnancy processes and leads to adverse effects.^17-18 One of the most common and immediate complications of maternal malaria is severe anemia. The infection leads to the destruction of red blood cells and the sequestration of infected erythrocytes in the placenta, causing a significant reduction in hemoglobin levels. Maternal anemia can result in fatigue, reduced oxygen transport to tissues, and increased susceptibility to other infections. The severity of anemia often correlates with the intensity of malaria infection and the level of placental damage, emphasizing the need for prompt diagnosis and treatment.^19-20 Maternal malaria is a significant risk factor for preterm birth. The infection-induced inflammation and immune response can lead to premature rupture of membranes and increased uterine contractions. Additionally, the placental damage caused by malaria can impair the placenta's ability to support fetal growth, leading to preterm delivery. Studies have consistently shown that women with malaria are at a higher risk of delivering before 37 weeks of gestation, which can have long-term consequences for neonatal health.^21-22 Low birth weight (LBW) is another immediate outcome associated with maternal malaria. The parasite's impact on the placenta can disrupt nutrient and oxygen transfer to the fetus, resulting in inadequate fetal growth. Infants born to mothers with malaria are more likely to be of low birth weight, which is a significant predictor of neonatal morbidity and mortality. LBW infants are at higher risk for respiratory distress, infections, and developmental delays, underscoring the importance of effective malaria management during pregnancy.^23-24 Placental dysfunction is a critical consequence of maternal malaria, affecting both maternal and fetal health. The sequestration of malaria-infected erythrocytes in the placenta leads to localized inflammation and damage. This damage impairs the placental structure and function, disrupting the exchange of nutrients and gases between mother and fetus. As a result, the placenta's ability to support the growing fetus is compromised, contributing to complications such as preterm birth and low birth weight.^25-26

Immune Response and Inflammation

The maternal immune response to malaria involves the release of pro-inflammatory cytokines and activation of immune cells. This inflammatory response is intended to combat the infection but can also have detrimental effects on pregnancy. Elevated levels of inflammatory markers in the placenta can lead to tissue damage and contribute to adverse outcomes such as preterm labor and fetal growth restriction.^27-28 Beyond fetal health, maternal malaria can significantly impact the health of the mother. Severe malaria can lead to complications such as severe anemia, acute respiratory distress syndrome, and even death. The overall health of the mother directly influences pregnancy outcomes, and severe complications can exacerbate the risks for both the mother and the fetus. Ensuring prompt and effective treatment of maternal malaria is essential for safeguarding both maternal and fetal health.^29-30 Accurate diagnosis and effective treatment of maternal malaria are critical for managing immediate pregnancy outcomes. The clinical presentation of malaria in pregnant women can be challenging, as symptoms may overlap with other pregnancy-related conditions. Rapid diagnostic tests and appropriate antimalarial therapies are essential for timely intervention. Addressing challenges in diagnosis and treatment is key to reducing the impact of maternal malaria on pregnancy outcomes.^31-32 The immediate consequences of maternal malaria underscore the importance of integrated malaria prevention and treatment strategies during pregnancy. Public health initiatives should focus on improving access to antenatal care, ensuring early diagnosis and treatment, and implementing preventive measures such as insecticide-treated bed nets. By addressing the immediate risks associated with maternal malaria, it is possible to improve pregnancy outcomes and reduce the burden of malaria on maternal and fetal health.^33-34

Impact on Placental Health

The placenta plays a critical role in supporting fetal development by facilitating the exchange of nutrients, gases, and waste products between the mother and the fetus. Maternal malaria, primarily caused by Plasmodium falciparum, significantly impacts placental health, leading to a range of complications that affect both maternal and fetal well-being.^35-36 One of the primary mechanisms through which maternal malaria affects the placenta is the sequestration of malaria-infected erythrocytes. These infected cells adhere to the endothelial cells of the placental blood vessels, leading to localized inflammation and vascular damage. This sequestration disrupts the normal flow of blood within the placenta, impairing nutrient and oxygen transfer to the fetus and causing placental dysfunction.^37-38 Maternal malaria triggers a strong inflammatory response in the placenta, characterized by the release of pro-inflammatory cytokines and the activation of immune cells. This inflammation can lead to tissue damage and interfere with the placenta's ability to perform its essential functions. Elevated levels of cytokines such as TNF-alpha and IL-6 are often observed in the placentas of malaria-infected women, contributing to inflammatory damage and dysfunction.^39-40 The infection and subsequent inflammatory response can lead to increased production of reactive oxygen species (ROS) within the placenta. Oxidative stress from ROS can damage cellular components, including lipids, proteins, and DNA. This oxidative damage exacerbates placental inflammation and impairs the structural and functional integrity of the placenta, further compromising its ability to support fetal growth.^41-42

Consequences for Placental Function

The damage inflicted by malaria on the placental blood vessels and the inflammatory response can severely impair the placenta's ability to transfer nutrients and oxygen to the fetus. This disruption in nutrient exchange can lead to fetal growth restriction, low birth weight, and other adverse outcomes. The compromised oxygen supply also increases the risk of hypoxia-related complications in the fetus.^43-44 Chronic malaria infections can lead to placental insufficiency, where the placenta is unable to meet the metabolic needs of the fetus. This condition often results from the cumulative effects of inflammatory damage, oxidative stress, and impaired blood flow. Placental insufficiency is associated with a range of complications, including preterm birth, intrauterine growth restriction, and stillbirth.^45-46 In severe cases of malaria, the placental damage can lead to structural malformations, such as placental infarcts and fibrosis. These abnormalities can further compromise placental function and contribute to adverse pregnancy outcomes. The presence of these malformations may indicate a more severe impact of malaria on placental health.^47-48

Impact on Fetal Development

The impaired nutrient and oxygen delivery due to placental dysfunction often results in fetal growth restriction. Infants born to mothers with malaria are more likely to be small for gestational age and have low birth weight. This growth restriction can have long-term consequences for neonatal health, including increased susceptibility to infections and developmental delays.⁴⁹ The inflammatory response and placental damage caused by malaria can increase the risk of preterm birth. The disruption of normal placental function and the premature rupture of membranes are key factors contributing to early delivery. Preterm birth carries risks such as respiratory distress syndrome and other complications that can affect the infant's health and development.⁵⁰ There is evidence suggesting that placental malaria can impact neurodevelopmental outcomes in infants. The combination of reduced oxygen supply and exposure to inflammatory cytokines may affect brain development, potentially leading to cognitive and behavioral issues later in life. Long-term studies are needed to fully understand the impact of placental malaria on neurodevelopmental outcomes.⁵¹

Strategies to Mitigate Placental Damage

Prompt and effective treatment of maternal malaria is crucial for minimizing placental damage. Antimalarial therapies, such as artemisinin-based combination therapies (ACTs), can help clear the infection and reduce inflammation, thereby mitigating the impact on placental health. Early diagnosis and treatment are key to preventing severe complications and preserving placental function.^52-53 Implementing preventive measures, such as the use of insecticide-treated bed nets and intermittent preventive treatment with sulfadoxine-pyrimethamine (IPTp), can help reduce the incidence of maternal malaria and protect placental health. These measures are particularly important in malaria-endemic regions to prevent infection and its associated complications.⁵⁴ Regular monitoring of pregnant women in malaria-endemic areas is essential for early detection and management of malaria. Comprehensive antenatal care, including ultrasound assessments and maternal health screenings, can help identify signs of placental dysfunction and guide appropriate interventions to protect both maternal and fetal health.⁵⁵

Mechanisms of Long-term Effects

Maternal malaria, particularly caused by Plasmodium falciparum, can have enduring impacts on both maternal and fetal health that extend beyond the immediate pregnancy. These long-term effects are mediated through several mechanisms that persist after the resolution of the acute infection. ⁵⁶ The inflammation and tissue damage caused by maternal malaria can result in chronic placental alterations, such as fibrosis and scarring. These structural changes can impair the placenta’s ability to function properly in future pregnancies. Persistent placental damage can lead to reduced nutrient and oxygen transfer, increasing the risk of complications such as fetal growth restriction and preterm birth in subsequent pregnancies.⁵⁷ Malaria-induced damage can disrupt the normal process of placental remodeling that occurs between pregnancies. The placenta undergoes dynamic changes to adapt to each pregnancy, but residual damage from previous infections can hinder this process. Incomplete or dysfunctional remodeling can affect the placenta's ability to support a healthy pregnancy, contributing to adverse outcomes in future gestations.⁵⁸

Maternal malaria induces a strong immune response characterized by the activation of pro-inflammatory pathways and cytokine production. This immune dysregulation can persist beyond the acute infection, potentially impacting future pregnancies. Altered immune responses can affect placental function and increase the risk of inflammatory complications in subsequent pregnancies.⁵⁹ Chronic changes in cytokine profiles, such as elevated levels of TNF-alpha and IL-6, may persist after malaria infection. These cytokines play a role in inflammation and immune response, and their prolonged elevation can contribute to a pro-inflammatory environment in the placenta during subsequent pregnancies. This persistent inflammation can exacerbate risks such as preterm labor and placental abruption.⁶⁰ Chronic inflammation resulting from past malaria infections can lead to ongoing tissue damage in the reproductive tract and placenta. This damage can impair normal physiological processes, such as blood flow and nutrient transfer, increasing the likelihood of complications in future pregnancies. The inflammatory environment may also affect the mother's ability to mount an appropriate response to new infections or stressors during subsequent pregnancies.⁶¹

Persistent inflammation can disrupt the immune system’s ability to maintain tolerance to the fetus, potentially leading to immune-related pregnancy complications. An inflammatory environment may increase the risk of conditions such as preterm birth or placental abruption by disrupting the balance between maternal and fetal immune responses.⁶² Oxidative stress caused by malaria-induced reactive oxygen species (ROS) can result in long-term cellular damage within the placenta. This residual oxidative damage may impair cellular function and contribute to persistent placental dysfunction. Over time, oxidative stress can lead to chronic health issues, affecting both maternal and fetal health in subsequent pregnancies.⁶³ The capacity of the placenta to repair oxidative damage may be compromised following a malaria infection. Persistent oxidative stress can overwhelm cellular repair mechanisms, leading to ongoing damage and dysfunction. This impaired repair capacity can affect the placenta’s ability to adapt and function optimally in future pregnancies.⁶⁴ Maternal malaria may induce epigenetic changes that affect gene expression in the placenta. These changes can result in altered expression of genes involved in inflammation, immune response, and placental function. Epigenetic modifications can persist beyond the acute infection, potentially influencing pregnancy outcomes in subsequent gestations.⁶⁵

Epigenetic changes induced by maternal malaria may be transmitted to the offspring, affecting their health and development. These inherited epigenetic marks can influence the child’s susceptibility to diseases and complications, potentially impacting their health throughout life.⁶⁶ The impact of maternal malaria on placental function and fetal development may result in developmental delays or cognitive impairments in offspring. Chronic exposure to a compromised placental environment can affect brain development and overall growth, leading to long-term health issues.⁶⁷ Children born to mothers with a history of malaria may be at increased risk of developing chronic conditions later in life. These conditions may include metabolic disorders, respiratory issues, or immune system dysfunction, reflecting the long-term impact of maternal malaria on developmental and health outcomes.⁶⁸ The long-term effects of maternal malaria underscore the importance of comprehensive maternal care strategies. Addressing both the immediate and long-term impacts of malaria is essential for improving reproductive health outcomes and reducing the burden of malaria on future pregnancies.⁶⁹ Implementing effective malaria prevention and treatment strategies, including insecticide-treated bed nets, intermittent preventive treatment, and early diagnosis, is crucial for mitigating the long-term effects of maternal malaria. Public health initiatives should focus on reducing the incidence of maternal malaria and improving overall maternal and fetal health.⁷⁰

Risk of Subsequent Pregnancy Complications

Maternal malaria, particularly caused by Plasmodium falciparum, can have significant long-term effects that extend beyond the immediate pregnancy. These effects may influence the outcomes of subsequent pregnancies, posing risks such as preterm birth, low birth weight, and other complications.⁷¹ Chronic damage to the placenta from a previous malaria infection can increase the risk of preterm birth in subsequent pregnancies. The residual scarring and fibrosis can impair placental function, leading to premature rupture of membranes and preterm labor. The inflammation and altered placental environment from prior infections can predispose the uterus to early contractions and premature delivery.⁷² Ongoing inflammation from past malaria infections can contribute to an increased risk of preterm birth. Persistent elevated levels of pro-inflammatory cytokines and immune dysregulation can trigger early labor. The inflammatory environment created by previous malaria episodes may disrupt normal uterine function, leading to preterm birth in future pregnancies.⁷³ Residual placental damage from maternal malaria can impair the placenta’s ability to efficiently transfer nutrients to the fetus, resulting in low birth weight in subsequent pregnancies. Inadequate nutrient supply due to impaired placental function can lead to fetal growth restriction, increasing the likelihood of delivering infants with low birth weight.⁷⁴ Fetuses exposed to a compromised placental environment in previous pregnancies may face developmental challenges that persist in subsequent pregnancies. The effects of prior nutrient and oxygen deprivation can influence fetal growth patterns, contributing to low birth weight and other related complications in future pregnancies.⁷⁵

Chronic inflammation resulting from past malaria infections can increase the risk of placental abruption in subsequent pregnancies. Inflammatory responses can lead to the formation of abnormal placental tissue and increased susceptibility to conditions such as premature detachment of the placenta from the uterine wall.⁷⁶ Residual damage and scarring from previous malaria infections can disrupt the structural integrity of the placenta, increasing the risk of placental abruption. Abnormalities in placental attachment and function can predispose the placenta to early separation, leading to complications such as bleeding and preterm delivery.⁷⁸ Women with a history of maternal malaria may experience altered immune responses in subsequent pregnancies, increasing their susceptibility to infections. This heightened vulnerability can exacerbate pregnancy complications and impact maternal health, potentially leading to adverse outcomes for both mother and fetus.⁷⁹ The chronic effects of malaria can contribute to the development of long-term health conditions, such as cardiovascular disease or chronic kidney dysfunction, which may affect pregnancy outcomes. The presence of these chronic conditions can further complicate subsequent pregnancies, increasing the risk of adverse outcomes.⁸⁰

Children born to mothers with a history of malaria may be at risk for neurodevelopmental issues, including cognitive and behavioral challenges. The impact of placental damage and compromised fetal growth can have lasting effects on brain development, potentially influencing health outcomes later in life.⁸¹ There is evidence suggesting that exposure to a compromised placental environment may increase the risk of chronic diseases in offspring. Conditions such as metabolic syndrome, respiratory issues, and other long-term health problems may be linked to maternal malaria and its impact on fetal development.⁸² Addressing the risks associated with subsequent pregnancies requires comprehensive maternal health strategies. This includes improved access to prenatal care, monitoring for signs of complications, and implementing preventive measures to manage the long-term effects of maternal malaria. Ensuring timely and effective interventions can help mitigate risks and improve outcomes.⁸³ Preventive measures such as the use of insecticide-treated bed nets, intermittent preventive treatment with antimalarials, and regular antenatal screenings are crucial in reducing the incidence of maternal malaria and its long-term effects. Public health initiatives should focus on these strategies to protect maternal and fetal health across multiple pregnancies.⁸⁴

Public Health Implications

The long-term effects of maternal malaria on subsequent pregnancies underscore the need for robust public health strategies to mitigate risks and enhance maternal and fetal health. Addressing the challenges posed by maternal malaria requires a multifaceted approach that includes prevention, early detection, and comprehensive care.⁸⁵ The use of insecticide-treated bed nets is a cornerstone of malaria prevention in endemic regions. ITNs provide a protective barrier against mosquito bites and significantly reduce the incidence of malaria. Expanding access to and encouraging the use of ITNs among pregnant women can help reduce the incidence of maternal malaria and its associated risks.⁸⁶ Intermittent preventive treatment with sulfadoxine-pyrimethamine (IPTp) is recommended for pregnant women in malaria-endemic areas. IPTp helps prevent malaria by providing a prophylactic dose of antimalarial medication at scheduled intervals. Ensuring that pregnant women receive IPTp as part of their routine antenatal care can reduce the burden of malaria and its long-term effects on maternal and fetal health.⁸⁷

Comprehensive antenatal care is crucial for monitoring and managing the health of pregnant women, particularly those at risk of malaria. Regular screenings for malaria, along with prompt diagnosis and treatment, can help address acute infections and reduce the risk of complications. Strengthening antenatal care services to include malaria prevention and management is essential for improving pregnancy outcomes. Access to rapid diagnostic tests (RDTs) for malaria enables timely and accurate diagnosis of the disease. Early detection allows for prompt treatment, reducing the impact of malaria on maternal and fetal health. Ensuring that healthcare facilities in malaria-endemic areas are equipped with RDTs and trained personnel is critical for effective malaria management.⁸⁸ Women with a history of maternal malaria should receive ongoing health monitoring to assess the long-term effects on their reproductive health. Regular follow-ups can help identify and manage potential complications in subsequent pregnancies. Implementing protocols for long-term health monitoring can improve outcomes and address any residual health issues. Public health campaigns to raise awareness about the long-term effects of maternal malaria are important for educating women and healthcare providers. Information about the risks associated with previous malaria infections and the importance of preventive measures can empower women to take proactive steps in managing their health and pregnancy outcomes.⁸⁹

Investing in research to understand the long-term impacts of maternal malaria is crucial for developing targeted interventions and policies. Research can provide insights into the mechanisms linking malaria to subsequent pregnancy complications and identify effective strategies for prevention and management. Supporting research initiatives can inform evidence-based public health policies. Developing and implementing policies that integrate malaria prevention and management into maternal health programs is essential. Policies should focus on improving access to malaria prevention tools, enhancing antenatal care, and ensuring effective treatment for malaria-infected pregnant women. Collaborative efforts between governments, health organizations, and communities can drive policy changes and improve reproductive health outcomes.⁸⁷ Addressing socioeconomic factors that contribute to the prevalence of maternal malaria is important for reducing health disparities. Ensuring equitable access to healthcare services, preventive measures, and treatment can help mitigate the impact of malaria on vulnerable populations. Targeted interventions for low-income and high-risk communities can improve health outcomes and reduce the burden of malaria. Strengthening health systems in malaria-endemic regions is critical for effective malaria management. Investments in healthcare infrastructure, training of healthcare workers, and supply chain management can enhance the delivery of malaria prevention and treatment services. A robust health system can better support the needs of pregnant women and improve overall maternal and fetal health.⁸⁸ Addressing maternal malaria requires collaboration between various sectors, including health, education, and agriculture. Multi-sectoral approaches can enhance malaria prevention and control efforts, integrate malaria management into broader health programs, and address underlying factors contributing to malaria transmission. Engaging communities in malaria prevention and control efforts is crucial for achieving sustained impact. Community-based initiatives, such as awareness campaigns, distribution of ITNs, and local support for antenatal care, can empower individuals to take ownership of their health and contribute to reducing the incidence of maternal malaria.⁸⁹

Conclusion

Maternal malaria, particularly caused by Plasmodium falciparum, has significant implications for both immediate and long-term pregnancy outcomes. The impact of maternal malaria extends beyond the acute phase of infection, influencing subsequent pregnancies and contributing to a range of complications, including preterm birth, low birth weight, and placental abruption.  Addressing the risks associated with maternal malaria requires a comprehensive public health approach. Strengthening malaria prevention programs, including the use of insecticide-treated bed nets and intermittent preventive treatment, is essential for reducing the incidence of maternal malaria and protecting placental health. Enhancing maternal health services, such as improving antenatal care and ensuring access to rapid diagnostic tests, can facilitate early detection and management of malaria, minimizing its impact on pregnancy outcomes.

Long-term health monitoring for women with a history of maternal malaria, alongside educational campaigns and policy development, is crucial for addressing ongoing risks and improving reproductive health. Supporting research initiatives to better understand the long-term effects of maternal malaria and implementing evidence-based policies can drive improvements in maternal and fetal health outcomes. Addressing socioeconomic factors and strengthening health systems are key to reducing health disparities and improving access to malaria prevention and treatment. Multi-sectoral collaboration and community engagement play vital roles in achieving sustained impact and empowering individuals to take proactive steps in managing their health.

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33. Okorie HM, Obeagu EI, Obarezi HC, Anyiam AF. Assessment of some inflammatory cytokines in malaria infected pregnant women in Imo State Nigeria. International Journal of Medical Science and Dental Research. 2019;2(1):25-36.

34. Okorie HM, Obeagu EI, Eze EN, Jeremiah ZA. Assessment of some haematological parameters in malaria infected pregnant women in Imo state Nigeria. Int. J. Curr. Res. Biol. Med. 2018;3(9):1-4.

35. Nwosu DC, Obeagu EI, Ezenwuba C, Agu GC, Amah H, Ozims SJ, Nwanjo HU, Edward A, Izuchukwu IF, Amadike JN, Nwagwu AJ. Antioxidant status of children with Plasmodium falciparum malaria in Owerri municipal council of Imo state. Int. J. Curr. Res. Chem. Pharm. Sci. 2016;3(8):40-46.

36. Harrington WE, Kakuru A, Jagannathan P. Malaria in pregnancy shapes the development of foetal and infant immunity. Parasite immunology. 2019;41(3): e12573. https://doi.org/10.1111/pim.12573 PMid:30019470

37. Okamgba OC, Nwosu DC, Nwobodo EI, Agu GC, Ozims SJ, Obeagu EI, Ibanga IE, Obioma-Elemba IE, Ihekaire DE, Obasi CC, Amah HC. Iron Status of Pregnant and Post-Partum Women with Malaria Parasitaemia in Aba Abia State, Nigeria. Annals of Clinical and Laboratory Research. 2017;5(4):206.

38. Anyiam AF, Arinze-Anyiam OC, Omosigho PO, Ibrahim M, Irondi EA, Obeagu EI, Obi E. Blood Group, Genotype, Malaria, Blood Pressure and Blood Glucose Screening Among Selected Adults of a Community in Kwara State: Implications to Public Health. Asian Hematology Research Journal. 2022;6(3):9-17.

39. Madekwe CC, Madekwe CC, Obeagu EI. Inequality of monitoring in Human Immunodeficiency Virus, Tuberculosis and Malaria: A Review. Madonna University journal of Medicine and Health Sciences. 2022;2(3):6-15.

40. Offie DC, Ibekwe AM, Agu CC, Esimai BN, Okpala PU, Obeagu EI, Ufelle SA, Ogbonna LN. Fibrinogen and C-Reactive Protein Significance in Children Infected by Plasmodium falciparum Species in Enugu, Enugu State, Nigeria. Journal of Pharmaceutical Research International. 2021;33(15):1-8. https://doi.org/10.9734/jpri/2021/v33i1531280

41. Obeagu EI, Ogunnaya FU. PREGNANCYINDUCED HAEMATOLOGICAL CHANGES: A KEY TO MARTERNAL AND CHILD HEALTH. European Journal of Biomedical. 2023;10(8):42-43. 

42. Obeagu EI, Ofodile AC, Okwuanaso CB. A review of urinary tract infections in pregnant women: Risks factors. J Pub Health Nutri. 2023; 6 (1).2023;137:26-35

43. Obeagu EI, Obeagu GU, Musiimenta E. Post partum haemorrhage among pregnant women: Update on risks factors. Int. J. Curr. Res. Med. Sci. 2023;9(2): 14-17.DOI: https://doi.org/10.22192/ijcrms.2023.09.02.003 

44. Obeagu EI, Obeagu GU, Ogunnaya FU. Deep vein thrombosis in pregnancy: A review of prevalence and risk factors. Int. J. Curr. Res. Chem. Pharm. Sci. 2023;10(8): 14-21.DOI: 10.22192/ijcrcps.2023.10.08.002

45. Arama C, Quin JE, Kouriba B, Östlund Farrants AK, Troye-Blomberg M, Doumbo OK. Epigenetics and malaria susceptibility/protection: A missing piece of the puzzle. Frontiers in Immunology. 2018; 9:1733. https://doi.org/10.3389/fimmu.2018.01733 PMid:30158923 PMCid:PMC6104485

46. Okorie HM, Obeagu EI, Eze EN, Jeremiah ZA. Assessment of some haematological parameters in malaria infected pregnant women in Imo state Nigeria. Int. J. Curr. Res. Biol. Med. 2018;3(9): 1-4.DOI: https://doi.org/10.22192/ijcrbm.2018.03.09.001 

47. Onyenweaku FC, Amah HC, Obeagu EI, Nwandikor UU, Onwuasoanya UF. Prevalence of asymptomatic bacteriuria and its antibiotic susceptibility pattern in pregnant women attending private ante natal clinics in Umuahia Metropolitan. Int J Curr Res Biol Med. 2017;2(2): 13-23.DOI: https://doi.org/10.22192/ijcrbm.2017.02.02.003 

48. Okoroiwu IL, Chinedu-Madu JU, Obeagu EI, Vincent CC, Ochiabuto OM, Ibekwe AM, Amaechi CO, Agu CC, Anoh NV, Amadi NM. Evaluation of Iron Status, Haemoglobin and Protein Levels of Pregnant Women in Owerri Metropolis. Journal of Pharmaceutical Research International. 2021;33(27A):36-43. https://doi.org/10.9734/jpri/2021/v33i27A31491

49. Obeagu EI, Njar VE, Obeagu GU. Infertility: Prevalence and Consequences. Int. J. Curr. Res. Chem. Pharm. Sci. 2023;10(7):43-50.

50. Emeka-Obi OR, Ibeh NC, Obeagu EI, Okorie HM. Evaluation of levels of some inflammatory cytokines in preeclamptic women in owerri. Journal of Pharmaceutical Research International. 2021;33(42A):53-65. https://doi.org/10.9734/jpri/2021/v33i42A32384

51. Broen K, Brustoski K, Engelmann I, Luty AJ. Placental Plasmodium falciparum infection: causes and consequences of in utero sensitization to parasite antigens. Molecular and biochemical parasitology. 2007;151(1):1-8. https://doi.org/10.1016/j.molbiopara.2006.10.001 PMid:17081634

52. Okorie HM, Obeagu EI, Eze EN, Jeremiah ZA. Assessment of coagulation parameters in malaria infected pregnant women in Imo state, Nigeria. International Journal of Current Research in Medical Sciences. 2018;4(9):41-49.

53. Ogbonna LN, Ezeoru VC, Ofodile AC, Ochiabuto OM, Obi-Ezeani CN, Okpala PU, Okafor CJ, Obeagu GU, Busari AI, Obeagu EI. Gender Based Variations of Haematological Parameters of Patients with Asymptomatic Malaria in Akure, Ondo State, Nigeria. Journal of Pharmaceutical Research International. 2021;33(8):75-80. https://doi.org/10.9734/jpri/2021/v33i831216

54. Eberendu IF, Ozims SJ, Agu GC, Amah HC, Obasi CC, Obioma-Elemba JE, Ihekaire DE, Ibanga IE, Amah CC, Obeagu EI, Nwosu DC. Impact of human activities on the breeding of mosquitoes of human disease in Owerri metropolis, Imo state. Int J Adv Res Biol Sci IJARBS. 2017;4(12):98-106. https://doi.org/10.22192/ijarbs.2017.04.12.010

55. Obeagu EI, Ofodile AC, Okwuanaso CB. A review on socio economic and behavioral aspects of malaria and its control among children under 5 years of age in Africa. J Pub Health Nutri. 2023; 6 (1): 136.

56. Djontu JC, Siewe Siewe S, Mpeke Edene YD, Nana BC, Chomga Foko EV, Bigoga JD, Leke RF, Megnekou R. Impact of placental Plasmodium falciparum malaria infection on the Cameroonian maternal and neonate's plasma levels of some cytokines known to regulate T cells differentiation and function. Malaria journal. 2016; 15:1-1. https://doi.org/10.1186/s12936-016-1611-0 PMid:27871325 PMCid:PMC5117507

57. Obeagu EI, Faduma MH, Uzoma G. Ectopic Pregnancy: A Review. Int. J. Curr. Res. Chem. Pharm. Sci. 2023;10(4): 40-4.DOI: https://doi.org/10.22192/ijcrcps.2023.10.04.004 

58. Obeagu EI, Gamade SM, Obeagu GU. The roles of Neutrophils in pregnancy. Int. J. Curr. Res. Med. Sci. 2023;9(5): 31-35.DOI: https://doi.org/10.22192/ijcrms.2023.09.05.005 

59. Obeagu EI, Obeagu GU. Molar Pregnancy: Update of prevalence and risk factors. Int. J. Curr. Res. Med. Sci. 2023;9(7): 25-28.DOI: https://doi.org/10.19080/JGWH.2023.25.556169

60. Kabyemela E, Gonçalves BP, Prevots DR, Morrison R, Harrington W, Gwamaka M, Kurtis JD, Fried M, Duffy PE. Cytokine profiles at birth predict malaria severity during infancy. PloS one. 2013;8(10):e77214. https://doi.org/10.1371/journal.pone.0077214 PMid:24130857 PMCid:PMC3795067

61. Ibebuike JE, Ojie CA, Nwokike GI, Obeagu EI, Nwosu DC, Nwanjo HU, Agu GC, Ezenwuba CO, Nwagu SA, Akujuobi AU. Barriers to utilization of maternal health services in southern senatorial district of Cross Rivers state, Nigeria. International Journal of Advanced Multidisciplinary Research. 2017;4(8): 1-9.DOI: https://doi.org/10.22192/ijamr.2017.04.08.001 

62. Emannuel G, Martin O, Peter OS, Obeagu EI, Daniel K. Factors Influencing Early Neonatal Adverse Outcomes among Women with HIV with Post Dated Pregnancies Delivering at Kampala International University Teaching Hospital, Uganda. Asian Journal of Pregnancy and Childbirth. 2023;6(1):203-211. http://research.sdpublishers.net/id/eprint/2819/ .

63. Okorie HM, Obeagu EI, Eze EN, Jeremiah ZA. Assessment of coagulation parameters in malaria infected pregnant women in Imo state, Nigeria. International Journal of Current Research in Medical Sciences. 2018;4(9): 41-9.DOI: https://doi.org/10.22192/ijcrms.2018.04.09.006 

64. Obeagu EI, Obeagu GU. Postpartum haemorrhage among women delivering through spontaneous vaginal delivery: Prevalence and risk factors. Int. J. Curr. Res. Chem. Pharm. Sci. 2023;10(8): 22-6.DOI: https://doi.org/10.22192/ijcrcps.2023.10.08.003 

65. Obeagu E, Eze RI, Obeagu EI, Nnatuanya IN, Dara EC. ZINC LEVEL IN APPARENTLY PREGNANT WOMEN IN URBAN AREA. Madonna University journal of Medicine and Health Sciences. 2022;2(1):134-48. https://www.journal.madonnauniversity.edu.ng/index.php/medicine/article/view/40 .

66. Ogomaka IA, Obeagu EI. Malaria in Pregnancy Amidst Possession of Insecticide Treated Bed Nets (ITNs) in Orlu LGA of Imo State, Nigeria. Journal of Pharmaceutical Research International. 2021;33(41B):380-386. https://doi.org/10.9734/jpri/2021/v33i41B32377

67. Obeagu EI, Ogunnaya FU, Obeagu GU, Ndidi AC. SICKLE CELL ANAEMIA: A GESTATIONAL ENIGMA. migration. 2023; 17:18.

68. Harrington WE, Kakuru A, Jagannathan P. Malaria in pregnancy shapes the development of foetal and infant immunity. Parasite immunology. 2019;41(3):e12573. https://doi.org/10.1111/pim.12573 PMid:30019470

69. Ifeanyi OE, Uzoma OG. A review on erythropietin in pregnancy. J. Gynecol. Womens Health. 2018;8(3):1-4. https://www.academia.edu/download/56538560/A_Review_on_Erythropietin_in_Pregnancy.pdf . https://doi.org/10.19080/JGWH.2018.08.555740

70. Ifeanyi OE. A review on pregnancy and haematology. Int. J. Curr. Res. Biol. Med. 2018;3(5): 26-8.DOI: 10.22192/ijcrbm.2018.03.05.006

71. Nwosu DC, Nwanjo HU, Obeagu EI, Ibebuike JE, Ezeama MC. Ihekireh. Changes in liver enzymes and lipid profile of pregnant women with malaria in Owerri, Nigeria. International Journal of Current Research and Academic Review. 2015;3(5):376-383.

72. Ibebuike JE, Ojie CA, Nwokike GI, Obeagu EI, Nwosu DC, Nwanjo HU, Agu GC, Ezenwuba CO, Nwagu SA, Akujuobi AU. Factors that influence women's utilization of primary health care services in Calabar Cros river state, Nigeria. Int. J. Curr. Res. Chem. Pharm. Sci. 2017;4(7):28-33. https://doi.org/10.22192/ijcrcps.2017.04.07.006

73. Elemchukwu Q, Obeagu EI, Ochei KC. Prevalence of Anaemia among Pregnant Women in Braithwaite Memorial Specialist Hospital (BMSH) Port Harcourt. IOSR Journal of Pharmacy and Biological Sciences. 2014;9(5):59-64. https://doi.org/10.9790/3008-09525964

74. Natama HM, Moncunill G, Rovira-Vallbona E, Sanz H, Sorgho H, Aguilar R, Coulibaly-Traoré M, Somé MA, Scott S, Valéa I, Mens PF. Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life. BMC medicine. 2018; 16:1-5. https://doi.org/10.1186/s12916-018-1187-3 PMid:30384846 PMCid:PMC6214168

75. Akandinda M, Obeagu EI, Katonera MT. Non Governmental Organizations and Women's Health Empowerment in Uganda: A Review. Asian Research Journal of Gynaecology and Obstetrics. 2022;8(3):12-26.

76. Gamde MS, Obeagu EI. IRON DEFICIENCY ANAEMIA: ENEMICAL TO PREGNANCY. European Journal of Biomedical. 2023;10(9):272-275. 

77. Emeka-Obi OR, Ibeh NC, Obeagu EI, Okorie HM. Evaluation of levels of some inflammatory cytokines in preeclamptic women in owerri. Journal of Pharmaceutical Research International. 2021;33(42A):53-65. https://doi.org/10.9734/jpri/2021/v33i42A32384

78. Emeka-Obi OR, Ibeh NC, Obeagu EI, Okorie HM. Studies of Some Haemostatic Variables in Preeclamptic Women in Owerri, Imo State, Nigeria. Journal of Pharmaceutical Research International. 2021;33(42B):39-48. https://doi.org/10.9734/jpri/2021/v33i42B32402

79. Obeagu EI, Obeagu GU. Postpartum haemorrhage among women delivering through spontaneous vaginal delivery: Prevalence and risk factors. Int. J. Curr. Res. Chem. Pharm. Sci. 2023;10(8):22-26.

80. Obeagu EI, Obeagu GU. Sickle Cell Anaemia in Pregnancy: A Review. International Research in Medical and Health Sciences. 2023;6(2):10-13.

81. Mutabingwa TK, Bolla MC, Li JL, Domingo GJ, Li X, Fried M, Duffy PE. Maternal malaria and gravidity interact to modify infant susceptibility to malaria. PLoS medicine. 2005;2(12):e407. https://doi.org/10.1371/journal.pmed.0020407 PMid:16259531 PMCid:PMC1277932

82. Gamble C, Ekwaru PJ, Garner P, Ter Kuile FO. Insecticide-treated nets for the prevention of malaria in pregnancy: a systematic review of randomised controlled trials. PLoS medicine. 2007;4(3):e107. https://doi.org/10.1371/journal.pmed.0040107 PMid:17388668 PMCid:PMC1831739

83. Okoko BJ, Enwere G, Ota MO. The epidemiology and consequences of maternal malaria: a review of immunological basis. Acta tropica. 2003;87(2):193-205. https://doi.org/10.1016/S0001-706X(03)00097-4 PMid:12826295

84. Dobaño C, Berthoud T, Manaca MN, Nhabomba A, Guinovart C, Aguilar R, Barbosa A, Groves P, Rodríguez MH, Jimenez A, Quimice LM. High production of pro-inflammatory cytokines by maternal blood mononuclear cells is associated with reduced maternal malaria but increased cord blood infection. Malaria Journal. 2018; 17:1-3. https://doi.org/10.1186/s12936-018-2317-2 PMid:29743113 PMCid:PMC5944101

85. Umbers AJ, Stanisic DI, Ome M, Wangnapi R, Hanieh S, Unger HW, Robinson LJ, Lufele E, Baiwog F, Siba PM, King CL. Does malaria affect placental development? Evidence from in vitro models. PLoS One. 2013;8(1):e55269. https://doi.org/10.1371/journal.pone.0055269 PMid:23383132 PMCid:PMC3561386

86. Arama C, Quin JE, Kouriba B, Östlund Farrants AK, Troye-Blomberg M, Doumbo OK. Epigenetics and malaria susceptibility/protection: A missing piece of the puzzle. Frontiers in Immunology. 2018; 9:1733. https://doi.org/10.3389/fimmu.2018.01733 PMid:30158923 PMCid:PMC6104485

87. Gbedande K, Carpio VH, Stephens R. Using two phases of the CD 4 T cell response to blood‐stage murine malaria to understand regulation of systemic immunity and placental pathology in Plasmodium falciparum infection. Immunological reviews. 2020;293(1):88-114. https://doi.org/10.1111/imr.12835 PMid:31903675 PMCid:PMC7540220

88. Lindsay SW, Thomas MB, Kleinschmidt I. Threats to the effectiveness of insecticide-treated bednets for malaria control: thinking beyond insecticide resistance. The Lancet Global Health. 2021;9(9):e1325-1331. https://doi.org/10.1016/S2214-109X(21)00216-3 PMid:34216565

89. Akinleye SO, Falade CO, Ajayi IO. Knowledge and utilization of intermittent preventive treatment for malaria among pregnant women attending antenatal clinics in primary health care centers in rural southwest, Nigeria: a cross-sectional study. BMC pregnancy and childbirth. 2009; 9:1-9. https://doi.org/10.1186/1471-2393-9-28 PMid:19589164 PMCid:PMC2719593