• Users Online: 91
  • Print this page
  • Email this page

 Table of Contents  
Year : 2022  |  Volume : 6  |  Issue : 2  |  Page : 185-192

“Asymptomatic” plasmodium falciparum parasitemia and micronutrient deficiencies among pregnant women in Oyo State

1 Department of Medical Laboratory Science, Faculty of Basic Medical Sciences, Lead City University, Ibadan, Nigeria
2 Department of Medical Laboratory Science, School of Basic Medical Sciences, College of Medical Sciences, University of Benin, Benin, Nigeria

Date of Submission02-Oct-2021
Date of Acceptance20-Dec-2021
Date of Web Publication17-Jun-2022

Correspondence Address:
Mufutau Mosunmade Azeez
Department of Medical Laboratory Science, Faculty of Basic Medical Sciences, Lead City University, Ibadan
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/bbrj.bbrj_255_21

Rights and Permissions

Background: Plasmodium falciparum parasitemia coupled with nutritional deficiencies, especially relating to micronutrients in pregnancy, may be a recipe for adverse pregnancy outcomes. This study was conducted to determine the prevalence of asymptomatic P. falciparum infection and some micronutrient deficiencies among pregnant women in Oyo State. Methods: Three hundred and sixteen pregnant women aged 16–45 years and 100 apparently healthy nonpregnant women of the same age range serving as controls from the 3 senatorial districts of Oyo State were enrolled in this study after obtaining their consent. Blood samples were collected and examined for P. falciparum using RDT kit and Giemsa-stained film microscopy while the selected micronutrients – calcium, iron, copper, and zinc – were assayed with atomic absorption spectrophotometer. Results: P. falciparum was detected in 82 out of the 316 pregnant women studied representing a percentage prevalence of 25.95 while the prevalence rate was 1% (1 out of 100) among the nonpregnant control women (P < 0.0001). Factors that significantly impacted on P. falciparum prevalence were pregnancy status, age, gestational age, parity, and seasonal variations. Out of the 316 pregnant women studied, 27 (8.5%) and 35 (11.1%) were deficient in calcium and iron, respectively. However, 13 of the 82 parasitemic pregnant women (15.85%) had calcium micronutrient deficiency, with only 14 out 234 (5.98%) observed in nonparasitemic pregnant women (P < 0.0001). While 10 (12.19%) had iron deficiency among the parasitemic pregnant women, 25 (10.68%) had iron deficiency among the nonparasitemic pregnant women. The only parasitemic nonpregnant control out of the 100 had calcium and iron micronutrient deficiencies (100%) as against 24.24% and 20.24%, respectively, in nonparasitemic controls. Copper and zinc micronutrient deficiencies were not observed among the study subjects. Conclusion: Continuous health education with emphasis on compliance to dietary instructions and malaria prevention measures, monitoring parasitemic pregnant women till delivery, and including malaria testing in the routine laboratory tests for antenatal care are hereby advocated.

Keywords: Micronutrient deficiencies, Oyo State, Plasmodium falciparum, pregnant women

How to cite this article:
Azeez MM, Akinbo FO. “Asymptomatic” plasmodium falciparum parasitemia and micronutrient deficiencies among pregnant women in Oyo State. Biomed Biotechnol Res J 2022;6:185-92

How to cite this URL:
Azeez MM, Akinbo FO. “Asymptomatic” plasmodium falciparum parasitemia and micronutrient deficiencies among pregnant women in Oyo State. Biomed Biotechnol Res J [serial online] 2022 [cited 2023 Mar 26];6:185-92. Available from: https://www.bmbtrj.org/text.asp?2022/6/2/185/347710

  Introduction Top

Malaria represents a serious threat to health systems in sub-Saharan African where morbidity and mortality from it are the highest and inadequate surveillance systems to control its spread.[1] It remains one of the most important devastating infectious diseases and is caused by a protozoan parasite of the genus Plasmodium.[2],[3] Despite the global attention being given to it by the World Health Organization and other various national governments alone or in collaboration with nongovernmental organizations, its public health challenge is far from being over.[4]

The most vulnerable groups are incontrovertibly children of ages 0–5 years and pregnant women in their first and second pregnancy.[5] Pregnant women are three times more likely to suffer from severe disease as a result of malarial infection compared with their nonpregnant counterparts and have a mortality rate from severe disease that approaches 50%.[6],[7] Kovacs et al.[8] even reported that an estimated 100,000 and 10,000 neonatal and maternal deaths, respectively, occur yearly due to malaria in pregnancy. An estimated 54.7 million pregnancies occurred in areas of stable Plasmodium falciparum malaria transmission and an additional 70.5 million pregnancies in areas of low transmission or areas with only Plasmodium vivax in 2007.[9],[10] In Nigeria and other endemic areas, malaria is a major etiology of morbidity and mortality, particularly among pregnant women.[11],[12] Pregnant women become more susceptible to the infection because their immune response is suppressed by human chorionic gonadotropin and prolactin levels which are high in pregnancy.[13] This immunosuppression is necessary to prevent fetal rejection as a semi-allogeneic transplant.[14]

Malaria infection during pregnancy poses a substantial risk to the mother and her fetus (and the neonate). It is a major cause of severe maternal anemia and responsible for an estimated 30%–35% of low birth weight (LBW) babies and for 75,000–200,000 infant deaths.[15] Placental infection is very variable and ranges from 3.5% to 75% depending on the malaria epidemiology in the area and seasonal variation among others.[16] P. falciparum has been documented to be the only species that can colonize the human placenta.[15]

Micronutrient deficiencies have been established to be a contributory factor in abnormal prenatal development and/or pregnancy outcome, and the common micronutrients are Vitamins A, B, C, D, and E, calcium, iron, copper, zinc, and magnesium.[17] Adequate intake of micronutrients is a sine qua non for the development of efficient immune system.[18] Low-quality diet arising from inadequate intake of animal source foods, particularly in developing countries, has been observed to be a major predisposing factor in micronutrient deficiencies, while in the developed world, those consuming little or no meat and/or milk have been reported to have increased risk of micronutrient deficiencies as well.[19]

Findings from several studies have identified maternal undernutrition and P. falciparum infection as important recipes for adverse pregnancy outcomes. An estimated annual neonatal mortality of 800,000 has been attributed to undernutrition while malaria has been estimated to cause an estimated 900,000 low birth deliveries annually and over 100,000 infant mortality yearly.[20],[21]

There is an increasing evidence linking micronutrient deficiencies with malaria-caused P. falciparum, especially in developing countries like Nigeria where deficiencies in some micronutrients may be associated.[17] There is dearth of data on asymptomatic P. falciparum infection in association with micronutrient deficiency among pregnant women in the three senatorial districts of Oyo State, Nigeria. It is therefore against the foregoing that this study was undertaken to determine the prevalence of asymptomatic malaria and micronutrient deficiency among pregnant women in Oyo State.

  Materials and Methods Top

Study area

This study was carried out at three selected hospitals, namely Adeoyo Maternity Hospital, Ibadan (Oyo South senatorial district); State Hospital, Oyo (Oyo Central senatorial district); and State Hospital, Ogbomoso (Oyo North senatorial district).

Study population

Four hundred and sixteen (416) subjects made up of 316 consenting pregnant women attending antenatal clinics at the study sites and 100 apparently healthy age-matched nonpregnant women as controls were enrolled in this study. The age of participants ranged from 16 to 45 years. Pregnant women with asymptomatic malaria, those attending these health facilities as well as pregnant women that consented were included in this study. Pregnant women on antimalarial therapy, those not registered for antenatal care, and pregnant women that refused consent were excluded from this study. A structured questionnaire was administered to collect biodata and sociodemographic information which included age, parity, gestational age, educational status, occupation, and residential area among others. The protocol for this study was approved by the Ethics and Research Committee of Oyo State Ministry of Health, Ibadan.

Specimen collection

About 10 ml of venous blood was collected from each of the participants with 4 ml being dispensed into ethylenediaminetetraacetic acid bottle and mixed gently while the remaining 6 ml was dispensed into plain bottle, allowed to clot, centrifuged after retraction to separate serum. The sera were kept frozen at −20°C until analyzed.

Specimen processing

Malaria parasite detection was conducted using SD Bioline RDT kit (05FK80) for P. falciparum/P. vivax according to the manufacturer's instructions. Thick and thin blood films were made and stained for 30 min with 10% Giemsa stain and rinsed with buffer solution. The stained blood films were allowed to air-dry and examined microscopically under bright light using oil immersion objective. The thick films were used for parasite detection and density estimation, whereas the thin films were used for speciation of parasite.[22]

Full blood count was conducted using autoanalyzer Sysmex Kx-21 (Sysmex Corporation, Kobe, Japan). Anemia was determined using hemoglobin (Hb) concentration of <11 g/dl for pregnant women.[23]

The micronutrients assayed for were calcium, iron, copper, and zinc using atomic absorption spectrophotometer (AAS) (Buck Scientific 210 VGP, East Norwalk, CT). Briefly, for each of the analytes, the AAS was auto-zeroed using the flame from the lowest to the highest calibration. The corresponding absorbance was obtained and the graph of absorbance against concentration of the micronutrients was read in parts per million (ppm).[24]

Statistical analysis

The frequency data were analyzed using Chi-square test (χ2), while the potential risk factors were analyzed using the odds ratios. The statistical software used was INSTAT® (GraphPad Software Inc., La Jolla, CA, USA).

  Results Top

A prevalence of 25.95% asymptomatic P. falciparum infection was observed among pregnant women in this study, an indication that pregnancy status significantly affected malaria infection among pregnant women in Oyo State (P < 0.0001). Pregnancy status was significantly associated with P. falciparum infection among pregnant women in Oyo State (odds ratio [OR] = 34.692; 95% confidence interval [CI] = 4.760, 252.86; P < 0.0001) [Table 1].
Table 1: Prevalence of Plasmodium falciparum infection among pregnant and nonpregnant women

Click here to view

Pregnant women from Ibadan had the highest prevalence of P. falciparum infection (33. 91%), followed by those from Oyo town (32.97%), whereas the least (10%) was observed from Ogbomoso. The study site significantly affected the prevalence of P. falciparum infection among pregnant women (P < 0.0001) [Table 2].
Table 2: Relationship between study site and Plasmodium falciparum infection among pregnant women

Click here to view

Age of pregnant women strongly affected the prevalence of P. falciparum infection in Oyo State (P < 0.0001), with those that are 21–25 years' age group having the highest prevalence (46.7%) when compared with other age groups [Table 3].
Table 3: Effects of risk factors among pregnant women infected with Plasmodium falciparum in Oyo state

Click here to view

Gestational age strongly affected P. falciparum infection among pregnant women (P = 0.0148), with 40% occurring during the first trimester, while 20.9% and 26.1% occurred in the second and third trimesters, respectively [Table 4].
Table 4: Influence of anemia and platelet count on the prevalence of Plasmodium falciparum infection among pregnant women in Oyo State

Click here to view

Primiparous pregnant women had the highest prevalence of P. falciparum infection (42.3%) when compared with the multiparous pregnant women (12.2%). In addition, parity strongly affected the prevalence of P. falciparum infection among pregnant women in Oyo State (OR = 5.285; 95% CI = 3.007, 9.286; P < 0.0001).

Seasonal variation was associated strongly with the prevalence of P. falciparum infection among pregnant women in Oyo State (P < 0.0001) as the prevalence of P. falciparum infection was higher (39.6%) during the raining season compared with the dry season (24.5%).

Educational and occupational status did not significantly impact on the prevalence of malaria infection among pregnant women in Oyo State.

Anemia strongly impacted on the prevalence of P. falciparum infection among pregnant women in this study (OR = 3.474; 95% CI = 1.981, 6.092; P < 0.0001). Pregnant women with anemia had the highest prevalence of P. falciparum infection (46.5%) compared with those without anemia (20%). Participants with thrombocytopenia (platelet count <157 × 103) were more infected with P. falciparum in this study (51.3%). Furthermore, platelet count below 157 × 103/mm3 was strongly associated with P. falciparum infection among pregnant women in Oyo State (OR = 0.1226; 95% CI = 0.0695, 0.2164; P < 0.0001).

Out of the 82 pregnant women with P. falciparum infection, 13 (15.85%) were deficient of calcium while only 14 (5.98%) of the nonparasitemic pregnant women had calcium deficiency [Table 5]. Iron deficiency (12.19%) was observed among pregnant women, whereas 10.68% of iron deficiency was detected in the nonparasitemic pregnant women. Deficiency of copper and zinc was not observed among the parasitemic pregnant women [Table 5].
Table 5: Distribution of micronutrient deficiency among pregnant women infected with Plasmodium falciparum

Click here to view

There was only one case each observed with deficiencies in calcium and iron in the nonpregnant control women [Table 6].
Table 6: Distribution of micronutrient deficiency in nonpregnant control women

Click here to view

  Discussion Top

The interrelationship between pregnancy and P. falciparum infection may serve as recipe for adverse outcomes that impact on the mother and the fetus.[25],[26] This association may equally be potentiated by micronutrient deficiencies which have been implicated in unpleasant health outcomes such as preterm birth, LBW, maternal anemia, maternal and perinatal mortality, intrauterine growth retardation, altered immune competency, and cognitive deficits in the newborn.[17],[20],[27],[28],[29] To the best of our knowledge, this is the first study in recent times in the selected study sites to assess asymptomatic P. falciparum infection and micronutrient deficiency status in pregnant women.

In this study, only P. falciparum was recovered among pregnant women in Oyo State. Similar observations have been made by Akinboye et al.[30] among febrile pregnant women in Ibadan and Awosolu et al.[31] in a cross-sectional study in urban communities of Ibadan. Pregnancy has been shown to favor P. falciparum malaria transmission as a result of predisposition to reduced immunity due to general immunosuppression sustained by elevated level of cortisol which allows fetal allograft retention but renders the women susceptible to various infectious diseases.[32] A prevalence of 25.95% P. falciparum infection was observed among pregnant women in this study. The nonpregnant subjects had a prevalence of 1%. Pregnancy status significantly impacted on the acquisition of P. falciparum infection in this study (P < 0.0001). The prevalence observed in our study is similar to that observed by Akinbo et al.[17] that reported 27.9% among pregnant women in Owo, Ondo State; 26.7% by Muhammad et al.[33] among pregnant women in Yaqshid district of Somalia, and 24% reported by Douamba et al.[34] among pregnant women in Ouagadougou. The reason for this finding may be due to the prevailing socioeconomic and environmental factors in these developing countries. It is, however, significantly lower than the prevalence of 41.6% in Northeastern Nigeria,[35] 58% among Nigerian pregnant women,[36] and 59.9% in a rural community in Eastern Nigeria.[37] The difference in prevalence in our study and that of others may be attributable to improvement in malaria prevention, treatment, and control measures and compliance over the years in our study sites.

Lack of education, nonavailability or inadequacy of drainage systems, and inaccessibility of basic healthcare facilities affect the quality of health and prevalence of diseases in different communities.[38] The location of this study is a significant factor in the variation of the prevalence observed in our study sites (P < 0.0001), with 33.91% in Ibadan and 32.97% in Oyo compared with the observed 10% in Ogbomoso. This may be a reflection of differences in malaria transmission intensity and geographical and environmental factors as earlier espoused by Kweku et al.[39] and Tegegne et al.[38] including socioeconomic variables. Availability, affordability, and effective usage of preventive measures across different communities may also be a contributory factor.

Data from this study indicate that the age of pregnant women significantly affected the prevalence of P. falciparum infection, with participants that are 21–25 years old having the highest prevalence (46.7%) (P < 0.0001). This may actually be a reflection of parity as most of the subjects in that age group were actually primiparous who would naturally experience some level of immunosuppression due to pregnancy which makes them more susceptible to infectious agents including malaria parasites. Pregnancy brings about changes in physiological and immunological dynamics leading to modulation of pro-inflammatory responses and decreases immune system mechanism of the mother to prevent the rejection of the fetus as a semi-allogeneic transplant.[14],[40]

Gestational age impacted significantly on the occurrence of asymptomatic P. falciparum infection among pregnant women in this study (P = 0.0148). The highest prevalence of P. falciparum infection among pregnant women in their first trimester found in this study is consistent with reports from several studies across different geographical areas that observed gestational age as a risk factor for acquiring malaria,[25],[37] especially in the first trimester. Based on the preponderance of opinions that malaria in early pregnancy increases the risk of adverse pregnancy outcomes after organogenesis and placentation,[17],[41] a significant number of pregnant women in this study may be at risk of adverse pregnancy outcomes.

Parity in pregnancy has been shown through several studies in malaria endemic areas in the tropics to be a significant factor in the occurrence of higher prevalence of P. falciparum infection in primigravidae than in multigravidae.[42],[43],[44] This fact is consistent with the finding in this study which showed a significant difference in the prevalence of P. falciparum infection between primiparous and multiparous among pregnant women in Oyo State (P < 0.0001). This observation is similar to the reports from other studies in Nigeria.[17],[42],[44] It has been observed that based on avalanche of reports including the current study, malaria prevalence reduces with increasing gravidity. The decrease in asymptomatic P. falciparum infection in multiparous women could be suggestive of the development of preimmunity to malaria with increased parity, whereas primiparous remain susceptible due to partial development of immunity[44] or lack of specific immunity to placenta malaria acquired during previous malaria episode.[45] This immunity is said to accumulate with successive pregnancies, provided there is exposure to P. falciparum infection.[21] This may explain the reason for our finding.

Raining season provides a recipe for ecological and environmental alterations favoring the breeding of mosquito vector and thereby enhancing transmission intensity of the parasite.[46] Inadequate waste disposal facilities, lack of adequate drainage systems, and poor standard of living may also be considered as contributory factors.[47] Seasonal variation was strongly associated with P. falciparum infection among pregnant women in Oyo State (P < 0.0001). This observation is in consonance with reports from other studies that reported higher malaria infection during raining season in Western Cameroon and Northern Mali.[48],[49]

In this study, educational status did not impact malaria parasite infection significantly (P = 0.2546) among pregnant women in Oyo State, though there were variations in the prevalence of P. falciparum across levels of educational status which is in agreement with the report of Dawaki et al.[50] among Hausa communities in Kano. Pregnant women with primary or no formal education had more infections than those with secondary and tertiary education because higher levels of education were associated with improved knowledge and practice about appropriate strategies for the prevention and treatment of malaria[51] while those at the lower rung of the educational ladder may lack adequate knowledge of malaria causation and effective application of preventive methods.

It has been observed that being a farmer may increase the risk of P. falciparum infection in sub-Saharan Africa.[52] Occupational status did not significantly influence the prevalence of malaria infection among pregnant women in Oyo State (P = 0.098). However, traders had the highest P. falciparum infection, followed by artisans and those with formal employment, respectively, whereas the full-time homemakers had the least. The comparative low prevalence of P. falciparum infection in pregnant women that are full-time homemakers may not be surprising based on their less exposure to the outside environment where more mosquitoes abound when compared to the other occupational groups. It is noteworthy to mention that none of the participants in this study indicated farming as occupation which could have increased the probability of higher prevalence of malaria due to increased hazards of exposure to malaria vectors in the farmlands. Conversely, occupation was reported to have a significant impact on malaria occurrence[53] as farming laborers had more chances of getting infected than salaried/business individuals in Bargi PHC, Jabalpur district, Central India.

Site of residence appeared to influence the malaria parasitemia in our study as those in urban and GRA had less infections: 17.7% and 8.53%, respectively, whereas the rural dwellers had the highest (74.39%) but not statistically significant (P = 0.5996). Our finding is also in consonance with general expectation that malaria infection should be higher in rural than in urban settings.[42] There is concurrence in the prevalence observed in this study among the GRA residents and that of urban residents in Kaduna which may be an indication of similar environmental practices of adequate drainage, sanitation, and maintenance of relatively clean residential surroundings. The relatively high incidence of parasitemia in the urban city centers when compared with GRA in this study may be attributed to congested environment due to unplanned urbanization, general apathy to malaria prevention measures, poor drainage system, and sanitation.

Hematological parameters are considered a hallmark of malaria and are reported to be most pronounced in P. falciparum malaria infections;[54] these however vary between pregnant and nonpregnant women due to physiological changes controlled by hormonal (estrogen and progesterone) influences.[55] Anemia strongly impacted on the prevalence of P. falciparum infection among pregnant women in Oyo State (P < 0.0001) where pregnant women with anemia had the highest prevalence of 46.5% of P. falciparum infection when compared with those without anemia (20%). Studies from other climes have shown anemia among pregnant women infected with P. falciparum with Ouma et al.[56] reporting a 70% anemia among pregnant women in urban/peri-urban areas of Kisumu, Western Kenya, with malaria being the most important determinant. This report is in consonance with the widely known fact that anemia is the most common complication of P. falciparum infection.[44] Thrombocytopenia has been observed to be common in malaria infection.[54],[57],[58],[59] Similar observation was reported in our study where pregnant women with platelet count <157 × 103/mm3 had the highest prevalence of P. falciparum infection (51.3%) when compared with those with platelet count >157 × 103/mm3 (11.42%). Platelet count below 157 × 103/mm3 significantly affected the prevalence of P. falciparum infection in this study (P < 0.0001). This may be due to the fact that platelets and coagulation factors are vital components of the extraordinary complex environment that surrounds flowing or sequestrated parasitized erythrocytes and the enclosing tubular vascular endothelium.[60]

Trace elements are the key elements of complex enzymes responsible for the modulation of antioxidant defense system of an organism[61] and are closely associated with fetal growth and development.[62] Iron which can easily be obtained from meat, fish, legumes, and vegetables[63] plays an important role in the production of Hb and oxygenation of erythrocytes and lymphocytes while equally improving the functions of enzymes in protein metabolism and enhances the functions of copper (Cu) and calcium (Ca). It is also needed for the metabolism of B complex vitamins.[64] Iron deficiency causes anemia which affects about 22% of women of child-bearing age in Europe and as much as 50% in developing countries[65] Calcium is the main component of the teeth and skeleton, and it plays an important role in the activation of muscle-keeping, nervous excitement and enzyme activation.[62] Copper protects cells from the toxic superoxide anion and ensures normal fetal growth and immune function while also participating in the maintenance of normal hematopoietic function and maintenance of central nervous system.[66] Zinc is a component of a variety of enzymes and nucleic acid and is directly involved in the body's synthesis of DNA and RNA and transcription and replication which plays an important role in the human immune system and the development of fetal nervous system.[67] There is a growing body of evidence linking micronutrient deficiencies and malaria incidence or severity arising mostly from P. falciparum endemic areas,[68] and deficiencies of micronutrients such as zinc, copper, iron, and calcium are much more common in developing countries.[69] This assertion is, however, not supported by our reports as copper and zinc deficiencies were not observed in the pregnant women with asymptomatic P. falciparum parasitemia, whereas only one case each was recorded in the control group that had calcium and iron deficiency, respectively. However, 15.98% and 12.19% of pregnant women in Oyo State had calcium and iron deficiencies, respectively. Our findings of low micronutrient deficiencies may be a reflection of improved dietary compliance by pregnant women to antenatal care advice on nutritional issues over the years. Similar observation of low deficiency of micronutrients in pregnancy was reported elsewhere.[62],[70] These calcium and iron deficiencies observed from our data are in sharp contrast to the reports of Asaolu and Igbaakin[64] and Akinbo et al.[17] that observed higher deficiencies of calcium and iron among pregnant women. Based on the documented evidence of proven antiplasmodial activity of some plants like Securidaca longepedunculata,[71] prophylactic usage of medicinal plant extracts with antimalarial properties may be considered as replacement or complimentary for SP currently in use for IPTP.

  Conclusion Top

Notwithstanding the adoption of IPTP, the relatively high prevalence of 25.95% asymptomatic P. falciparum infection was reported in pregnant women in comparison with 1% in nonpregnant women population, an indication that pregnancy status is a significant risk factor. Pregnant women within the age group of 21–25 years had a higher prevalence (46.7%) than others. Gestational age (with higher prevalence [40%] being observed in the first trimester) and parity (42.3% primiparous) and seasonal variation (highest in raining season-39.6%) were observed to have impacted significantly. Pregnant women with anemia had malaria infection prevalence of 46.5%, while those with thrombocytopenia had a prevalence of 51.3%. MND involving only calcium and iron with relatively low prevalence was also observed while anemia and thrombocytopenia were relatively more common in the parasitemic subjects. Continuous health education with emphasis on compliance to dietary instructions and malaria prevention measures, monitoring parasitemic pregnant women till delivery, and including malaria testing in the routine laboratory tests for antenatal care are hereby advocated.


We are indebted in gratitude to the managements of Adeoyo Maternity Hospital, Ibadan; State Hospital, Oyo; and State Hospital, Ogbomoso, especially the laboratory and ANC staffs for specimen collection and other supports while also appreciating most sincerely the consenting participants.

Financial support and sponsorship


Conflicts of interest

The authors declare that none of the authors have any competing interests.

  References Top

Bazie VB, Ouattara AK, Sagna T, Compaore TR, Soubeiga ST, Sorgho PA, et al. Resistance of Plasmodium falciparum to sulfadoxine-pyrimethamine (Dhfr and Dhps) and artemisinin and its derivatives (K13): A major challenge for malaria elimination in West Africa. J Biosci Med 2020;8:82-95.  Back to cited text no. 1
Adeoye FA. Improving Laboratory-Based Diagnosis of Malaria: Malaria Microscopy Methods Manual. 1st ed. Surulere, Lagos: Edoson Publishers; 2016.  Back to cited text no. 2
Osei M, Ansah F, Matrevi SA, Asante KP, Awandare GA, Quashie NB, et al. Amplification of GTP-cyclohydrolase 1 gene in Plasmodium falciparum isolates with the quadruple mutant of dihydrofolate reductase and dihydropteroate synthase genes in Ghana. PLoS One 2018;13:e0204871.  Back to cited text no. 3
World Health Organization. World Malaria Day 2018: Ready to Beat Malaria; 2018. Available from: http://www.who.int. [Last accessed on 2021 Oct 02].  Back to cited text no. 4
Federal Ministry of Health (FMOH). National Guidelines for Diagnosis and Treatment of Malaria. Federal Ministry of Health, Abuja, Nigeria; 2014.  Back to cited text no. 5
Monif GR, Baker DA, editors. Infectious Disease in Obstetrics and Gynaecology. 6th ed. New York: Parthenon; 2004. p. 280-6.  Back to cited text no. 6
World Health Organization. World Malaria Report, 2016. Available from: http://www.who.int/malaria/publications/world-malaria-report-20156/en/. [Last accessed on 2016 Dec 28].  Back to cited text no. 7
Kovacs SD, Rijken MJ, Stergachis A. Treating severe malaria in pregnancy: A review of the evidence. Drug Saf 2015;38:165-81.  Back to cited text no. 8
Dellicour S, Hall S, Chandramohan D, Greenwood B. The safety of artemisinins during pregnancy: A pressing question. Malar J 2007;6:15.  Back to cited text no. 9
Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: A demographic study. PLoS Med 2010;7:e1000221.  Back to cited text no. 10
Wernsdorfer WH, Payne D. Drug sensitivity tests in malaria parasites. In: Wernsdorfer WH, McGregor IA, editors. Malaria: Principles and Practice of Malariology. Edinburgh: Churchill Livingstone; 1988.  Back to cited text no. 11
USAID President's Malaria Initiative Nigeria. Malaria Operational Plan FY; 2016. Available from: https://www.pmi.gov/docs/default-source/default-document-library/malaria-operational-plans/fy16/fy-2016-nigeria-malaria-operational-plan.pdf?sfvrn=13. [Last accessed on 2017 Feb 13].  Back to cited text no. 12
Myles D, Traser M, Cooper A. Change and adaptation in pregnancy: Immunity. In: Textbook of Midwives. 14th ed. UK: Churchill Livingstone; 2003. p. 197.  Back to cited text no. 13
Hountohotegbe T, Gbedande K, Agbota G, Ibitokou S, Massougbodji A, Deloron P, et al. Circulating cytokines associated with poor pregnancy outcomes in beninese exposed to infection with Plasmodium falciparum. Infect Immun 2020;88:e00042-20.  Back to cited text no. 14
Coll O, Menendez C, Botet F, Dayal R, World Association of Perinatal Medicine Perinatal Infections Working Group, Carbonell-Estrany X, et al. Treatment and prevention of malaria in pregnancy and newborn. J Perinat Med 2008;36:15-29.  Back to cited text no. 15
Menendez C, Ordi J, Ismail MR, Ventura PJ, Aponte JJ, Kahigwa E, et al. The impact of placental malaria on gestational age and birth weight. J Infect Dis 2000;181:1740-5.  Back to cited text no. 16
Akinbo FO, Alabi LO, Aiyeyemi JA. Micronutrient deficiencies among pregnant women with Plasmodium falciparum infection in Owo, Ondo State, Nigeria. Afr J Clin Exp Microbiol 2019;20:127-36.  Back to cited text no. 17
Maggini S, Wintergerst ES, Beveridge S, Hornig DH. Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. Br J Nutr 2007;98 Suppl 1:S29-35.  Back to cited text no. 18
Allen LH. Biological mechanismsthat might underlie iron's effects on fetal growth and preterm birth. Am J Clin Nutr 2005;81:1206-2012.  Back to cited text no. 19
Black RE, Victora CG, Walker SP, Bhutta ZA, Christian P, de Onis M, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013;382:427-51.  Back to cited text no. 20
Walker PG, Griffin JT, Cairns M, Rogerson SJ, van Eijk AM, ter Kuile F, et al. A model of parity-dependent immunity to placental malaria. Nat Commun 2013;4:1609.  Back to cited text no. 21
Cheesbrough M. District Laboratory Practices for Tropical Countries. Vol. I. New Delhi, India: Jaypee Brothers Medical Publishers Ltd.; 2005. p. 120-4.  Back to cited text no. 22
Beutler E, Waalen J. The definition of anemia: What is the lower limit of normal of the blood hemoglobin concentration? Blood 2006;107:1747-50.  Back to cited text no. 23
Nmorsi OP, Akwandu NC, Egwunyanga AO. Antioxidant status of Nigerian children with Plasmodium falciparum malaria. Afr J Microbiol Res 2007;1:61-4.  Back to cited text no. 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;20:573.  Back to cited text no. 25
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.  Back to cited text no. 26
Burke RM, Leon JS, Suchdev PS. Identification, prevention and treatment of iron deficiency during the first 1000 days. Nutrients 2014;6:4093-114.  Back to cited text no. 27
Peña-Rosas JP, De-Regil LM, Garcia-Casal MN, Dowswell T. Daily oral iron supplementation during pregnancy. Cochrane Database Syst Rev 2015:CD004736.  Back to cited text no. 28
Gernand AD, Schulze KJ, Stewart CP, West KP Jr., Christian P. Micronutrient deficiencies in pregnancy worldwide: Health effects and prevention. Nat Rev Endocrinol 2016;12:274-89.  Back to cited text no. 29
Akinboye OO, Okonofua CC, Awodele O, Agbolade OM, Ayinde OO, Rebacca SN, et al. The influence of malaria on some haematological parameters in pregnancy. Niger J Parasitol 2011;32:187-91.  Back to cited text no. 30
Awosolu OB, Yahaya ZS, Farah Haziqah MT, Simon-Oke IA, Fakunle C. A cross-sectional study of the prevalence, density, and risk factors associated with malaria transmission in urban communities of Ibadan, Southwestern Nigeria. Heliyon 2021;7:e05975.  Back to cited text no. 31
Meeusen EN, Bischof RJ, Lee CS. Comparative T-cell responses during pregnancy in large animals and humans. Am J Reprod Immunol 2001;46:169-79.  Back to cited text no. 32
Muhammad F, Yarow AM, Hossain MA, Chowdury GS, Ferdows KG. Prevalence of Plasmodium falciparum among pregnant women in Yaqshid District of Somalia. Daffodil Intern Univ J Allied Health Sci 2016;3:61-8.  Back to cited text no. 33
Douamba Z, Bisseye C, Djigma FW, Compaoré TR, Bazie VJ, Pietra V, et al. Asymptomatic malaria correlates with anaemia in pregnant women at Ouagadougou, Burkina Faso. J Biomed Biotechnol 2012;2012:198317.  Back to cited text no. 34
Kagu MB, Kawuwa MB, Gadzama GB. Anaemia in pregnancy: A cross-sectional study of pregnant women in a Sahelian tertiary hospital in Northeastern Nigeria. J Obstet Gynaecol 2007;27:676-9.  Back to cited text no. 35
Nwagha UI, Ugwu VO, Nwagha TU, Anyaehie BU. Asymptomatic Plasmodium parasitaemia in pregnant Nigerian women: Almost a decade after Roll Back Malaria. Trans R Soc Trop Med Hyg 2009;103:16-20.  Back to cited text no. 36
Ogbodo SO, Nwagha UI, Okaka AN, Ogenyi SC, Okoko RO, Nwagha TU. Malaria parasitaemia among pregnant women in a rural community of eastern Nigeria; need for combined measures. Niger J Physiol Sci 2009;24:95-100.  Back to cited text no. 37
Tegegne Y, Asmelash D, Ambachew S, Eshetie S, Addisu A, Jejaw Zeleke A. The prevalence of malaria among pregnant women in Ethiopia: A systematic review and meta-analysis. J Parasitol Res 2019;2019:8396091.  Back to cited text no. 38
Kweku M, Webster J, Taylor I, Burns S, Dedzo M. Public-private delivery of insecticide-treated nets: A voucher scheme in Volta Region, Ghana. Malar J 2007;6:14.  Back to cited text no. 39
Zen M, Ghirardello A, Iaccarino L, Tonon M, Campana C, Arienti S, et al. Hormones, immune response, and pregnancy in healthy women and SLE patients. Swiss Med Wkly 2010;140:187-201.  Back to cited text no. 40
Huynh BT, Cottrell G, Cot M, Briand V. Burden of malaria in early pregnancy: A neglected problem? Clin Infect Dis 2015;60:598-604.  Back to cited text no. 41
Aliyu MM, Nasir IA, Umar YA, Vanstawa AP, Medugu JT, Emeribe AU, et al. Prevalence, risk factors, and antimalarial resistance patterns of falciparum plasmodiasis among pregnant women in Kaduna metropolis, Nigeria. Ci Ji Yi Xue Za Zhi 2017;29:98-103.  Back to cited text no. 42
van Eijk AM, Ayisi JG, ter Kuile FO, Misore AO, Otieno JA, Rosen DH, et al. Risk factors for malaria in pregnancy in an urban and peri-urban population in western Kenya. Trans R Soc Trop Med Hyg 2002;96:586-92.  Back to cited text no. 43
Uneke CJ, Iyare FE, Sunday-Adeoye H, Ajayi JA. Evaluation of maternal malaria at childbirth using rapid diagnostic test and its relationship with birthweight and fetal haemoglobin levels in Nigeria. Int J Obstet Gynecol 2008;10:2-7.  Back to cited text no. 44
Staalsoe T, Shulman CE, Bulmer JN, Kawuondo K, Marsh K, Hviid L. Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria. Lancet 2004;363:283-9.  Back to cited text no. 45
Hoshen MB, Morse AP. A weather-driven model of malaria transmission. Malar J 2004;3:32.  Back to cited text no. 46
Erhabo O, Mohammed HJ, Ahmed HM, Ezimah AC. Effect of Plasmodium parasitaemia on some haematological parameters in children living in Sokoto, North Western, Nigeria. Int J Clin Med Res 2014;1:57-64.  Back to cited text no. 47
Atangana J, Fondjo E, Fomena A, Tamesse JL, Patchoke S, Ndjemai HN, et al. Seasonal variations of malaria transmission in Western Cameroon highlands: Entomological, parasitological and clinical investigations. J Cell Anim Biol 2009;3:033-8.  Back to cited text no. 48
Koita OA, Sangaré L, Sango HA, Dao S, Keita N, Maiga M, et al. Effect of seasonality and ecological factors on the prevalence of the four malaria parasite species in northern Mali. J Trop Med 2012;2012:367160.  Back to cited text no. 49
Dawaki S, Al-Mekhlafi HM, Ithoi I, Ibrahim J, Atroosh WM, Abdulsalam AM, et al. Is Nigeria winning the battle against malaria? Prevalence, risk factors and KAP assessment among Hausa communities in Kano State. Malar J 2016;15:351.  Back to cited text no. 50
Dike N, Onwujekwe O, Ojukwu J, Ikeme A, Uzochukwu B, Shu E. Influence of education and knowledge on perceptions and practices to control malaria in Southeast Nigeria. Soc Sci Med 2006;63:103-6.  Back to cited text no. 51
Degarege A, Fennie K, Degarege D, Chennupati S, Madhivanan P. Improving socioeconomic status may reduce the burden of malaria in sub Saharan Africa: A systematic review and meta-analysis. PLoS One 2019;14:e0211205.  Back to cited text no. 52
Sharma RK, Singh MP, Saha KB, Bharti PK, Jain V, Singh PP, et al. Socio-economic & household risk factors of malaria in tribal areas of Madhya Pradesh, central India. Indian J Med Res 2015;141:567-75.  Back to cited text no. 53
[PUBMED]  [Full text]  
Kotepui M, Piwkham D, PhunPhuech B, Phiwklam N, Chupeerach C, Duangmano S. Effects of malaria parasite density on blood cell parameters. PLoS One 2015;10:e0121057.  Back to cited text no. 54
Adesina KT, Balogun OR, Babatunde AS, Sanni MA, Fadeyi A, Aderibigbe S. Impact of malaria parasitaemia on haematological parameters in pregnant women at booking in Ilorin, Nigeria. Trends Med Res 2009;4:84-90.  Back to cited text no. 55
Ouma P, van Eijk AM, Hamel MJ, Parise M, Ayisi JG, Otieno K, et al. Malaria and anaemia among pregnant women at first antenatal clinic visit in Kisumu, western Kenya. Trop Med Int Health 2007;12:1515-23.  Back to cited text no. 56
Jadhav UM, Patkar VS, Kadam NN. Thrombocytopenia in malaria-correlation with type and severity of malaria. J Assoc Physicians India 2004;52:615-8.  Back to cited text no. 57
Shaikh MA, Ahmed S, Diju IU, Dur-E-Yakta. Platelet count in malaria patients. J Ayub Med Coll Abbottabad 2011;23:143-5.  Back to cited text no. 58
Osaro E, Abdulrahaman A, Erhabor T. Effects of malaria parasitaemia on some haematological parameters of pregnant women of African Descent in Specialist Hospital, Sokoto, North Western Nigeria. JOJ Nurse Care 2019;10:555795.  Back to cited text no. 59
Abdalla SP. Malaria: A Haematological Perspective. London, UK: Imperial College Press; 2004. p. 21-7.  Back to cited text no. 60
Lewicka I, Kocyłowski R, Grzesiak M, Gaj Z, Oszukowski P, Suliburska J. Selected trace elements concentrations in pregnancy and their possible role – Literature review. Ginekol Pol 2017;88:509-14.  Back to cited text no. 61
Shen PJ, Gong B, Xu FY, Luo Y. Four trace elements in pregnant women and their relationships with adverse pregnancy outcomes. Eur Rev Med Pharmacol Sci 2015;19:4690-7.  Back to cited text no. 62
Marangoni F, Cetin I, Verduci E, Canzone G, Giovannini M, Scollo P, et al. Maternal diet and nutrient requirements in pregnancy and breastfeeding. An Italian Consensus Document. Nutrients 2016;8:629.  Back to cited text no. 63
Asaolu MF, Igbaakin PA. Serum levels of micronutrients and antioxidants during malaria in pregnant women in Ado-Ekiti, Ekiti State, Nigeria. Int J Med Med Sci 2009;1:523-36.  Back to cited text no. 64
Stevens GA, Finucane MM, De-Regil LM, Paciorek CJ, Flaxman SR, Branca F, et al. Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995-2011: A systematic analysis of population-representative data. Lancet Glob Health 2013;1:e16-25.  Back to cited text no. 65
Ergaz Z, Guillemin C, Neeman-Azulay M, Weinstein-Fudim L, Stodgell CJ, Miller RK, et al. Placental oxidative stress and decreased global DNA methylation are corrected by copper in the Cohen diabetic rat. Toxicol Appl Pharmacol 2014;276:220-30.  Back to cited text no. 66
Dickinson N, Rankin J, Pollard M, Maleta K, Robertson C, Hursthouse A. Evaluating environmental and social influences on iron and zinc status of pregnant subsistence farmers in two geographically contrasting regions of Southern Malawi. Sci Total Environ 2014;500-501:199-210.  Back to cited text no. 67
Benzecry SG, Alexandre MA, Vítor-Silva S, Salinas JL, de Melo GC, Marinho HA, et al. Micronutrient deficiencies and Plasmodium vivax malaria among children in the Brazilian Amazon. PLoS One 2016;11:e0151019.  Back to cited text no. 68
Stephenson LS, Latham MC, Ottesen EA. Global malnutrition. Parasitology 2000;121 Suppl: S5-22.  Back to cited text no. 69
Huang HM, Leung PL, Sun DZ, Zhu MG. Hair and serum calcium, iron, copper, and zinc levels during normal pregnancy at three trimesters. Biol Trace Elem Res 1999;69:111-20.  Back to cited text no. 70
Nguta JM. In vivo antimalarial activity, toxicity and phytochemical composition of total extracts from Securidaca longepedunculata Fresen. (Polygalaceae). Biomed Biotechnol Res J 2019;3:196-201.  Back to cited text no. 71
  [Full text]  


  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Materials and Me...
Article Tables

 Article Access Statistics
    PDF Downloaded77    
    Comments [Add]    

Recommend this journal