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 Table of Contents  
ORIGINAL ARTICLE
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
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/bbrj.bbrj_255_21

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  Abstract 


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 2022 Jun 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

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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

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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

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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

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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

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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

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  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.

Acknowledgments

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

Nil.

Conflicts of interest

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



 
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