|Year : 2018 | Volume
| Issue : 2 | Page : 59-65
Effect of placental malaria on placental and neonatal birthweight of primigravidae in Southeastern Nigeria
Festus Ehigiator Iyare1, Chigozie Jesse Uneke2
1 Department of Pathology, Ebonyi State University/Federal Teaching Hospital, Abakaliki, Ebonyi, Nigeria
2 Department of Medical Microbiology and Parasitology/Director, Directorate of Research, Innovation and Commercialization, Ebonyi State University, Abakaliki, Ebonyi, Nigeria
|Date of Web Publication||25-Feb-2019|
Dr. Festus Ehigiator Iyare
Department of Pathology, Ebonyi State University/Federal Teaching Hospital, PMB 102, Abakaliki 480001, Ebonyi
Source of Support: None, Conflict of Interest: None
Background: Adolescent primigravidae have increased risk of pregnancy associated complications and this is compounded by placental malaria in endemic areas. Placental weight is an acceptable marker of placental functional capacity and it correlates closely with birth weight which is recognized as an indicator of intrauterine growth. Methods: The study was done on primigravidae with uncomplicated singleton term pregnancy who fulfilled the inclusion criteria. Malaria parasites were tested for by microscopy of Giemsa stained thick and thin blood films on the matched pairs of mother and placental blood samples. Results: The total number of participants was 106 with mean age of 26 ± 0.553 years. Heavy weight placenta defined as placenta weight >750 g, accounted for 6.6% of which 42.8% had malaria. The mean placental weight, birth weight, and placenta weight ratio were 580.5 g, 2.87 kg and 0.207 respectively. Placental malaria accounted for 25% of the low birth weight. Conclusion: The maternal age at first pregnancy and delivery has significant impact on the placental weight ratio even more so among the adolescent primigravidae. Malaria induces placental hypertrophy with high placental ratio and reduced availability of nutrients to the growing foetus.
Keywords: Adolescent primigravidae, low-birth-weight, placental hypertrophy, placental malaria, placental weight ratio
|How to cite this article:|
Iyare FE, Uneke CJ. Effect of placental malaria on placental and neonatal birthweight of primigravidae in Southeastern Nigeria. Niger J Exp Clin Biosci 2018;6:59-65
|How to cite this URL:|
Iyare FE, Uneke CJ. Effect of placental malaria on placental and neonatal birthweight of primigravidae in Southeastern Nigeria. Niger J Exp Clin Biosci [serial online] 2018 [cited 2022 Aug 17];6:59-65. Available from: https://www.njecbonline.org/text.asp?2018/6/2/59/252844
| Background|| |
Pregnancies at the extremes of the reproductive age create new challenges in obstetric care as adolescent and older mothers have increased the risk of pregnancy-associated complications such as low-birth-weight, fetal death, preeclampsia, and preterm delivery.,, In Nigeria, 23% of women aged 15–19 are already mothers or pregnant with their first child.
It is generally agreed that a properly functioning placenta is vital for a successful pregnancy and failure of the placenta to gain weight and insufficiency of its function can result in fetal disorders. Size at birth is determined by two important factors, that is, placental function and duration of pregnancy. The placental function is difficult to assess; however, placental weight is a crude marker of placental size but correlates closely to birth weight in normal pregnancy and is widely used as a parameter of placental functional capacity,
Birth weight is used as an indicator of intrauterine growth and it is associated with long-term effects on health and disease in adult life. Low-birth-weight is the most commonly used measure of pregnancy outcome and is the single greatest risk factor for neonatal and infant mortality, poor neurosensory, cognitive, and behavioral development as well as for limited school performance and academic achievement. It is also a well-established risk factor for adverse long-term health, particularly cardiovascular diseases and metabolic syndromes in adult life. Large placenta and low-birth-weight have been implicated as factors predicting high blood pressure in adulthood.,,
Placental malaria is a major preventable cause of low-birth-weight, and it is estimated that 200,000 children die as a result of placental malaria associated low-birth-weight every year. Pregnant women are more attractive to mosquitoes and malaria is most frequent in first pregnancy with a higher risk of adverse outcome. Malaria is endemic in Nigeria with a prevalence of 919/100,000 population and remains one of the leading causes of morbidity and mortality accounting for 30% and 11% of child and maternal deaths, respectively., Pregnant women are three times more likely to suffer severe disease as a result of malarial infections compared with their nonpregnant colleagues and have a mortality rate from a severe disease that approaches 50%.
Throughout pregnancy, the size of the placenta changes and remains highly correlated with birth weight. Small placentas generally give rise to small babies. Studies have shown that adolescent and elderly mothers have increased the risk of delivering babies that are small for gestational age; and as placental weight and birth weight are closely correlated, it is expected that these mothers also have smaller placentas.,, Infant birth weight in primigravidae is frequently lower than subsequent births and pregnancy in adolescent girls is commonly associated with suboptimal fetal growth.
Thus, it seems that placenta of small size gives rise to low-birth-weight infants and patients with placental malaria have infants of low-birth-weight. It is also seems that primigravidae and adolescents frequently have high malarial parasitemia and produce low-birth-weight infants. Consequently, we hypothesize that placental weight in adolescents and elderly primigravidae with malaria are likely to be smaller and have low-birth-weight infants.
| Materials and Methods|| |
The study was conducted in Abakaliki, the capital of Ebonyi State, South-East Nigeria, from June 2006 to December 2006 at the former Ebonyi State University Teaching Hospital (EBSUTH) (now Federal Teaching Hospital Abakaliki), one of the largest health institutions in the region. South East geopolitical zone of Nigeria is one of the most densely populated areas of the country with a population of 16.5 million people, 11.7% of the national census and a population density of 402/km2 compared to 96/km2 for the country, majority of which are women (2006 census). Malaria transmission in the area is perennial, but usually at its peak toward the end of the rainy season.
Ethical approval was obtained from the Ethical Committee of the then EBSUTH, Abakaliki. No ethical issues arose during the study as placentae are routinely disposed off in the hospital.
Study population/Sampling technique
Primigravidae who presented themselves at the labor ward at full term for delivery of their babies at EBSUTH and fulfilled the following study inclusion criteria were enrolled in the study. (i) Attended antenatal clinic at EBSUTH, (ii) had an uncomplicated term singleton gestation, (iii) reside in Abakaliki and neighboring local government areas, (iv) had no obvious clinical evidence of malaria (asymptomatic), and (v) had no known underlying chronic illness. Just immediately after delivery, the placenta was collected immediately after expulsion and incision made on the maternal surface and the blood welling up was aspirated into a sterile ethylenediaminetetraacetic acid container for laboratory analysis. The placenta was then weighed fresh with the membranes and umbilical cord using the electronic weighing machine in grams. The baby weight was measured using the electronic weighing machine in kilograms. All other derivable measurements were obtained from the respective formulae.
Definition of terms
- Low-birth-weight is defined as baby weight <2500 g
- Heavyweight placenta is defined as placenta weight >750 g
- Normal weight placenta is defined as placenta weight 330–750 g
- Low weight placenta is defined as placenta weight <330 g.
The placental blood samples were analyzed for malaria parasite infection by performing the microscopy of Giemsa stained thick and thin films. The plus system was used for the determination of parasite density as previously outlined. All the films were double-checked blindly by experienced parasitologist, and if there were differences an additional assessment was made by another observer, and the average of the two agreeing counts using the plus system was recorded. Parasitemia was graded as 1–10 parasites per 100 thick film fields (“+” or 4–40 parasites per mm3), 11–100 parasites per 100 thick film fields (“++” or 41–400 parasites per mm3), and 1–10 parasites per single thin film fields (“+++” or 41–400 parasites per mm3).
Data are presented as mean ± standard error of the mean. Simple descriptive statistical analysis and Students' t-test for paired data were used to analyze the difference between the means of the groups. P < 0.05 was considered to be statistically significant.
| Results|| |
During the period, a total of 106 primigravidae were recorded out of 250 consecutive deliveries representing 42% of deliveries at the hospital. The mean age of the patients was 26 ± 0.553 years with the youngest being 16 years and the oldest being 43 years. The mean placental weight, mean birth weight, and mean placental ratio for the patients were 580.5 ± 18.59 g, 2.87 ± 0.0804 kg, and 0.207 ± 0.067, respectively [Table 1]. Adolescents, defined as women of 20 years of age and below, accounted for 18.9% of the patients and had higher mean placental weight (583.0 ± 33.75 g) compared to their nonadolescent counterparts (573.3 ± 28.49 g) but lower mean birth weight (2.76 ± 0.122 kg) compared to the nonadolescent women (2.89 ± 0.138 g) [Table 1]. Of all the 106 primigravidae screened, the prevalence of low-birth-weight was 22.6% and it was more common among the adolescents compared to the older age groups at 30% and 21%, respectively [Table 1].
|Table 1: Distribution of mean placental weight, birth weight, and placental weight ratio among the adolescent and nonadolescent primigravidae|
Click here to view
Seven (6.6%) of the placentas were classified as heavy, that is, it weighed more than 750 g, whereas 3 (2.8%) that is, placentas <330 g were low weight placentas [Table 2]. All the low weight placentas had no malaria, whereas 3 (42.8%) of the heavy placentas had malaria. A total of 32 (33.3%) of the normal weight placentas had malaria infection [Table 2].
|Table 2: Classification of placental weight and distribution of placental malaria|
Click here to view
The prevalence of placental malaria was 33% [Table 3]. The mean placental weight and mean birth weight of patients with malaria (594.6 ± 18.79 g; 2.94 ± 0.085 kg) were higher than those of patients without placental malaria (566.5 ± 18.37 g; 2.80 ± 0.076 kg) [Table 3]. Placental malaria accounted for 25.7% of the low-birth-weight infants [Table 3].
|Table 3: Effect of malaria on placental weight, birth weight, and placental ratio in primigravidae|
Click here to view
Of the 20 adolescent primigravidae screened, 7 (35%) had placental malaria, whereas of the 86 nonadolescent counterparts screened, 28 (32.5%) were infected with placental malaria [Table 4]. The mean placental weight of the adolescents with placental malaria was higher than those of the nonadolescents with placental malaria (658.56 ± 58.16 g vs. 578.57 ± 17.90 g) [Table 4]. However, the mean birth weight of the adolescents with placental malaria was considerably lower than that of the nonadolescents with placental malaria (2.58 ± 0.22 kg vs. 3.03 ± 0.08 kg) [Table 4].
|Table 4: Effect of malaria and age at pregnancy on placental weight, birth weight and placenta/birth weight ratio among primiparous women|
Click here to view
The age at first pregnancy and delivery had no statistically significant influence on the placental weight and birth weight but has significant impact on the placental weight ratio such that those in the nonadolescent age group have lower placental weight ratio of 0.186, that is, a smaller placenta with a high-birth-weight compared to the adolescents who had larger placentas with low-birth-weight and therefore high placental weight ratio [Table 1].
The placentas with malaria were quantitatively heavier than those without malaria, and the babies produced seem to be bigger with lower placental ratios. These differences were not statistically significant except in adolescents with placental malaria where the placental weight ratio was statistically significant [Table 2], [Table 3], [Table 4].
| Discussion|| |
Adolescents constitute a large proportion of all societies. They are restless, adventurous, with special health needs and are particularly vulnerable because of a lack of experience and immunity garnered from previous deliveries. They are usually forgotten or subsumed within maternal and childhood mortality and morbidity figures. This is even more so when global attention is focused mainly on mothers and under-five children. It is generally agreed that the efficient transfer of nutrients by the placenta is crucial to sustaining the normal development and survival of the fetus in utero.
This study has shown that primigravidae, especially adolescent primigravidae are more susceptible to placental malaria with higher prevalence of adverse pregnancy outcomes such as low-birth-weight. This conforms with the findings in many studies., In addition to this, there is associated placentomegaly and high placental weight ratio suggesting a less efficient placenta that has failed to translate its growth into proportionate fetal growth. Studies have also shown that in placental malaria, there is increased consumption of nutrients by the placenta, infiltrating mononuclear inflammatory cells that produce type-1 cytokines, trophozoites, and schizonts that sequester within the placenta such that the amount of nutrients available to the fetus is greatly reduced, In addition, there is increased thickening of the cytotrophoblastic membrane which may interfere with nutrient transport by the placenta, thereby further restricting the availability of nutrients to the growing fetus,
Thus it seems that the placental hypertrophy, reduced birth weight, and high placental weight ratio seen in this study may be an adaptive response by the placenta and fetus to the reduced availability of nutrients in utero. The mechanism underlying this observation is not yet determined, and it will require further investigation.
The age bracket, 21–25 years is recognized to represent the age of peak reproductive performance such that the effects of placental malaria or any perturbations of the fetoplacental environment are attenuated by their maturity, general reserves, and adaptability. This may explain their ability in maintaining a relatively more efficient placenta compared to those of the adolescent primigravidae and other older age groups. This is corroborated by this study where they have a lower placental weight ratio compared to the adolescents and the older age groups.
Our results show that the adolescent primigravidae have higher mean placental weight than their non-adolescent counterparts but lower mean birth weight compared to the nonadolescent women [Table 1]. This finding suggests that adolescent age may be a predisposing factor for low-birth-weight and that older mothers are more likely to have babies with higher birth weight. Harville et al. while studying the predictors of birth weight and gestational age among adolescents noted that older age at pregnancy was associated with higher birth weight. In addition to this, in a systematic review on maternal age as a risk factor for low-birth-weight, Aras observed that majority of the studies reviewed indicate that a very young maternal age is causally implicated with an increased risk of having LBW and preterm births. Although maternal age is known not to be the only factor responsible for low-birth-weight. The woman's health behavior during pregnancy, ethnicity, poverty status, age at menarche, maternal height, net maternal weight gain, and smoking during pregnancy can have independent effect on birth weight., However evidence from a number of studies have shown that after controlling for socioeconomic and obstetric risk factors, young age remains a risk factor for low-birth-weight.,,
The prevalence of placental malaria among the primigravidae studied was 33% [Table 2]. This outcome was comparatively higher than the results obtained in similar studies among primigravidae in Ibadan Nigeria (18.7%), and Kampala Uganda (19.6%). However, higher primigravidae placental malaria prevalence than what we obtained in our study was observed in Owerri Nigeria (36.3%), Dangme-West Ghana (50%), Nnewi Nigeria (65.8%), and Brong Ahafo Ghana (66.0%). These results suggest that the prevalence of placental malaria among primigravidae is high.
In a previous systematic review publication on placental malaria, it was clearly established that there exists a relationship between placental malaria and parity. Although a comparison was not made in our study between the primigravidae and multigravidae, several studies have observed that placental malaria prevalence was consistently higher in primigravidae compared to multigravidae, and in these studies, results were controlled for age.,, Some earlier studies conducted in malaria-endemic areas observed that, among several factors, parity independently influenced the placental malaria prevalence rate, with primigravidae having a two-to four-fold increased risk of placental malaria compared to multigravidae.,,
In this study, we observed that the prevalence of placental malaria was higher among adolescent mothers (35%) compared to their nonadolescent counterparts (32.5%) [Table 4]. In a previous study conducted in Yaoundé Cameroon, it was observed that among the significant risk factors for placental malaria using univariate analysis was being <20 years old. Similarly, in another previous study in Zaire, it was observed that mothers with malarious placentas were much younger than mothers with nonmalarious placentas. Immunological studies have shown that young women of child-bearing age may be more susceptible than older women to malaria because they are still in the process of acquiring natural immunity to malaria., In Blantyre, Malawi, Rogerson et al. in their study observed that after stratifying by gravidity, the associations between age and parasite prevalence were stronger than those between gravidity and prevalence after stratifying by age. They further noted that under conditions of low-to-moderate transmission, pregnancy-specific immunity is slow to develop, and age-related immunity may influence malaria prevalence in childbearing years.
There was a higher percentage of LBW babies (≤2.5 kg) among the adolescents (30%) compared to the non-adolescents (21%) [Table 1]. This outcome is consistent with the findings of several previous studies. In Mainland China, a higher risk for preterm birth and low-birth-weight neonates was observed among teenage group than among the older age group. Similarly, in Denizli, Turkey, and Kano Nigeria, teenage mothers had an increased incidence of preterm labor and low-birth-weight infants. Azevedo et al. in a systematic review of the literature on complications in adolescent pregnancy, observed that many studies indicated that the occurrence of premature births, low-weight newborns, or infants with very low weight and mortality was significantly greater among babies of adolescent mothers. However, in Caen, France, higher prevalence of prematurity and low-birth-weight in infants born to teenagers were not attributable to young maternal age after adjustment for confounding factors. Although many of the studies reviewed by Azevedo et al. showed that low-birth-weight was more common among adolescent mothers, they noted that the low-birth-weight may have been caused by the low number of prenatal visits, late initiation of prenatal care, inappropriate prenatal care, and other factors, such as low level of schooling, and poverty. This was supported by the report of Vieira et al. who noted that an association between maternal age and adverse outcomes was observed only in adolescent mothers with inadequate prenatal care, adding that adolescent mothers and their newborns are exposed to greater risk of adverse outcomes when prenatal care fails to comply with current guidelines. In addition to this, Omole-Ohonsi and Attah noted from their study of obstetric outcome of teenage pregnancy in Kano Nigeria, that teenage mothers who receive good family and community support, timely quality antenatal care and deliver in the hospital, should expect the similar obstetric outcome to that of their older peers.
There was also a higher percentage of LBW babies (≤2.5 kg) among the mothers with placental malaria (25.7%) compared to mothers without placental malaria (21.1%) [Table 3]. This finding is consistent with a number of previous studies which consistently showed that placental malaria is associated with higher risk of delivering low-birth-weight babies, However, the mean birth weight and mean placental weight of babies from mothers with placental malaria in our study was higher (2.94 kg ± 0.085 and 594.6 g ± 18.79) than mean birth weight and mean placental weight of babies from mothers without placental malaria (2.80 kg ± 0.076 and 566.5 g ± 18.37). This is contrary to the findings from some recent studies which indicated that the mean birth weight of babies born to mothers with placental malaria was lower than mean birth weight of babies born to mothers without placental malaria.,
Although placental malaria may directly affect birth weight by causing a mechanical compromise of placental circulation through widespread trophoblast basement thickening, increased fibrinoid necrosis and cytrophoblast prominence or indirectly interfere with placental functions and/or induce pathological lesions. This usually leads to reduced birth weight. However, in this study, both birth weight and placental weight were increased in infected placentas. This finding is supported by an earlier study by Bulmer et al. in the Gambia.
Because of these conflicting findings, there is yet to be a general consensus as to the main mechanisms mediating reductions in birth weight in placental malaria. Moreover, when birth weight is stratified and related to the types of placental infections (chronic or active) in different studies, there were conflicting findings. More studies are needed to properly elucidate this.
| Conclusion|| |
The age at first pregnancy and delivery has no statistically significant influence on the placental weight and birth weight but has a significant impact on the placental weight ratio that is the efficiency of the placenta even more so among the adolescent primigravidae. Malaria induces placental hypertrophy with reduced efficiency and reduced availability of nutrients to the growing fetus. The prevalence of placental malaria and low-birth-weight among adolescent primigravidae is high and is associated with placental hypertrophy.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Saenger P, Czernichow P, Hughes I, Reiter EO. Small for gestational age: Short stature and beyond. Endocr Rev 2007;28:219-51.
Murphy VE, Smith R, Giles WB, Clifton VL. Endocrine regulation of human fetal growth: The role of the mother, placenta, and fetus. Endocr Rev 2006;27:141-69.
Belkacemi L, Nelson DM, Desai M, Ross MG. Maternal undernutrition influences placental-fetal development. Biol Reprod 2010;83:325-31.
Auta A. Demographic factors associated with insecticide treated net use among Nigerian women and children. N
Am J Med Sci 2012;4:40-4.
Guyatt HL, Snow RW. Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa. Clin Microbiol Rev 2004;17:760-9.
Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, et al.
Placental hypoxia during placental malaria. J Infect Dis 2008;197:757-65.
Rogerson SJ, Mwapasa V, Meshnick SR. Malaria in pregnancy: Linking immunity and pathogenesis to prevention. Am J Trop Med Hyg 2007;77:14-22.
Roland MC, Friis CM, Voldner N, Godang K, Bollerslev J, Haugen G, et al.
Fetal growth versus birthweight: The role of placenta versus other determinants. PLoS One 2012;7:e39324.
Kenny LC, Lavender T, McNamee R, O'Neill SM, Mills T, Khashan AS, et al.
Advanced maternal age and adverse pregnancy outcome: Evidence from a large contemporary cohort. PLoS One 2013;8:e56583.
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.
Risnes KR, Romundstad PR, Nilsen TI, Eskild A, Vatten LJ. Placental weight relative to birth weight and long-term cardiovascular mortality: Findings from a cohort of 31,307 men and women. Am J Epidemiol 2009;170:622-31.
Aras RY. Is maternal age risk factor for low birth weight? Arch Med Health Sci 2013;1:33-7. [Full text]
Harville EW, Madkour AS, Xie Y. Predictors of birth weight and gestational age among adolescents. Am J Epidemiol 2012;176 Suppl 7:S150-63.
Fouelifack FY, Tameh TY, Mbong EN, Nana PN, Fouedjio JH, Fouogue JT, et al.
Outcome of deliveries among adolescent girls at the Yaoundé central hospital. BMC Pregnancy Childbirth 2014;14:102.
World Health Organization. Basic Malaria Microscopy. Learner's Guide. Geneva: World Health Organization; 1991.
Oduola AM, Phillips JH, Spicer SS, Galbraith RM. Plasmodium berghei
: Histology, immunocytochemistry, and ultrastructure of the placenta in rodent malaria. Exp Parasitol 1986;62:181-93.
Strobino DM, Ensminger ME, Kim YJ, Nanda J. Mechanisms for maternal age differences in birth weight. Am J Epidemiol 1995;142:504-14.
Swamy GK, Edwards S, Gelfand A, James SA, Miranda ML. Maternal age, birth order, and race: Differential effects on birthweight. J Epidemiol Community Health 2012;66:136-42.
Fraser AM, Brockert JE, Ward RH. Association of young maternal age with adverse reproductive outcomes. N
Engl J Med 1995;332:1113-7.
Akinbami LJ, Schoendorf KC, Kiely JL. Risk of preterm birth in multiparous teenagers. Arch Pediatr Adolesc Med 2000;154:1101-7.
Falade CO, Tongo OO, Ogunkunle OO, Orimadegun AE. Effects of malaria in pregnancy on newborn anthropometry. J Infect Dev Ctries 2010;4:448-53.
Namusoke F, Rasti N, Kironde F, Wahlgren M, Mirembe F. Malaria burden in pregnancy at Mulago national referral hospital in Kampala, Uganda. Mala Res Treat 2010;2010:1-10.
Ukaga CN, Nwoke BE, Udujih OS, Udujih OG, Ohaeri AA, Anosike JC, et al.
Placental malaria in Owerri, Imo state, South-Eastern Nigeria. Tanzan Health Res Bull 2007;9:180-5.
Ofori M, Ansah E, Agyepong I, Ofori-Adjei D, Hviid L, Akanmori B, et al.
Pregnancy-associated malaria in a rural community of Ghana. Ghana Med J 2009;43:13-8.
Oraneli BU, Okeke OC, Ubachukwu PO. Effect of placental malaria on birth weight of babies in Nnewi, Anambra state, Nigeria. J Vector Borne Dis 2013;50:13-7.
] [Full text]
Asante KP, Owusu-Agyei S, Cairns M, Dodoo D, Boamah EA, Gyasi R, et al.
Placental malaria and the risk of malaria in infants in a high malaria transmission area in Ghana: A prospective cohort study. J Infect Dis 2013;208:1504-13.
Uneke CJ. Impact of placental plasmodium falciparum malaria on pregnancy and perinatal outcome in sub-Saharan Africa: I: Introduction to placental malaria. Yale J Biol Med 2007;80:39-50.
Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke RF, et al.
Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg 2005;72:236-42.
Morgan HG. Placental malaria and low birthweight neonates in urban Sierra Leone. Ann Trop Med Parasitol 1994;88:575-80.
Cot M, Deloron P. Malaria prevention strategies. Br Med Bull 2003;67:137-48.
McGregor IA. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 1984;33:517-25.
McGregor IA, Wilson ME, Billewicz WZ. Malaria infection of the placenta in the Gambia, West Africa; its incidence and relationship to stillbirth, birthweight and placental weight. Trans R Soc Trop Med Hyg 1983;77:232-44.
Anagnos D, Lanoie LO, Palmieri JR, Ziefer A, Connor DH. Effects of placental malaria on mothers and neonates from Zaire. Z Parasitenkd 1986;72:57-64.
Oeuvray C, Theisen M, Rogier C, Trape JF, Jepsen S, Druilhe P, et al.
Cytophilic immunoglobulin responses to plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infect Immun 2000;68:2617-20.
Johnson AH, Leke RG, Mendell NR, Shon D, Suh YJ, Bomba-Nkolo D, et al.
Human leukocyte antigen class II alleles influence levels of antibodies to the plasmodium falciparum asexual-stage apical membrane antigen 1 but not to merozoite surface antigen 2 and merozoite surface protein 1. Infect Immun 2004;72:2762-71.
Rogerson SJ, van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, Molyneux ME, et al.
Malaria and anemia in antenatal women in Blantyre, Malawi: A twelve-month survey. Am J Trop Med Hyg 2000;62:335-40.
Liu X, Zhang W. Effect of maternal age on pregnancy: A retrospective cohort study. Chin Med J (Engl) 2014;127:2241-6.
Karabulut A, Ozkan S, Bozkurt AI, Karahan T, Kayan S. Perinatal outcomes and risk factors in adolescent and advanced age pregnancies: Comparison with normal reproductive age women. J Obstet Gynaecol 2013;33:346-50.
Omole-Ohonsi A, Attah RA. Obstetric outcome of teenage pregnancy in Kano, North-Western Nigeria. West Afr J Med 2010;29:318-22.
Azevedo WF, Diniz MB, Fonseca ES, Azevedo LM, Evangelista CB. Complications in adolescent pregnancy: Systematic review of the literature. Einstein (Sao Paulo) 2015;13:618-26.
de Vienne CM, Creveuil C, Dreyfus M. Does young maternal age increase the risk of adverse obstetric, fetal and neonatal outcomes: A cohort study. Eur J Obstet Gynecol Reprod Biol 2009;147:151-6.
Vieira CL, Coeli CM, Pinheiro RS, Brandão ER, Camargo KR Jr., Aguiar FP, et al.
Modifying effect of prenatal care on the association between young maternal age and adverse birth outcomes. J Pediatr Adolesc Gynecol 2012;25:185-9.
Kassam SN, Nesbitt S, Hunt LP, Oster N, Soothill P, Sergi C, et al.
Pregnancy outcomes in women with or without placental malaria infection. Int J Gynaecol Obstet 2006;93:225-32.
Ahmed R, Singh N, ter Kuile FO, Bharti PK, Singh PP, Desai M, et al.
Placental infections with histologically confirmed plasmodium falciparum are associated with adverse birth outcomes in India: A cross-sectional study. Malar J 2014;13:232.
Guin G, Shaw K, Khare S. Placental malaria prevalence of infestation amongst febrile pregnant women in central India: Maternal and perinatal outcome. J Obstet Gynaecol India 2012;62:25-31.
Moshi EZ, Kaaya EE, Kitinya JN. A histological and immunohistological study of malarial placentas. APMIS 1995;103:737-43.
Bulmer JN, Rasheed FN, Morrison L, Francis N, Greenwood BM. Placental malaria. II. A semi-quantitative investigation of the pathological features. Histopathology 1993;22:219-25.
[Table 1], [Table 2], [Table 3], [Table 4]