Abstract
Objective
To investigate the relationship between prenatal geophagy, maternal prenatal haematological indices, malaria, helminth infections and cognitive and motor development among offspring.
Methods
At least a year after delivery, 552 of 863 HIV-negative mothers with singleton births who completed a clinical trial comparing the efficacy of sulfadoxine-pyrimethamine and mefloquine during pregnancy in Allada, Benin, responded to a nutrition questionnaire including their geophageous habits during pregnancy. During the clinical trial, helminth infection, malaria, haemoglobin and ferritin concentrations were assessed at 1st and 2nd antenatal care visits (ANV) and at delivery. After the first ANV, women were administered daily iron and folic acid supplements until three what? post-delivery. Singleton children were assessed for cognitive function at age 1 year using the Mullen Scales of Early Learning.
Results
The prevalence of geophagy during pregnancy was 31.9%. Pregnant women reporting geophagy were more likely to be anaemic (AOR= 1.9, 95% CI [1.1, 3.4]) at their first ANV if they reported geophagy at the first trimester. Overall, prenatal geophagy was not associated with maternal haematological indices, malaria or helminth infections, but geophagy during the third trimester and throughout pregnancy was associated with poor motor function (AOR= −3.8, 95% CI [−6.9, −0.6]) and increased odds of geophageous behaviour in early childhood, respectively.
Conclusions
Prenatal geophagy is not associated with haematological indices in the presence of micronutrient supplementation. However, it may be associated with poor child motor function and infant geophagy. Geophagy should be screened early in pregnancy.
Keywords: geophagy, pica, anaemia, pregnancy, iron deficiency, child development
Introduction
Maternal, neonatal and child health has taken centre stage in the policies of several health systems around the world, especially in developing countries where maternal and infant mortality are highest [1]. In Africa, the drive towards improving maternal and child health has been steered by the millennium development goals (MDGs) 4 and 5: to reduce by two thirds, between 1990 and 2015, the under-five mortality rate and within this same period, to reduce by three-quarters the maternal mortality ratio[2]. This agenda is currently being furthered by the Strategic Development Goals to reduce global maternal deaths to 70 per 100,000 live births [3]. Notwithstanding the interventions aimed at reducing maternal and child morbidity and eventual mortality, and the strides made by these interventions, very little attention has been paid to nutritional habits of pregnant women, particularly pica, that could expose them and their offspring to adverse consequences.
Pica is the persistent craving and consumption of substances deemed non-nutritive by the consumer [4]. Common forms of pica include pagophagy (compulsive consumption of ice or freezer frosts), amylophagy (compulsive consumption of purified starch) and geophagy (compulsive consumption of earth, dirt or clay) [5]. The practice, which has been described since the days of Hippocrates (460–370 BC) persists in many parts of the world [6]. Geophagy in pregnancy has been reported even in some developed countries, mostly among minority groups in the United States [7]. The global prevalence of geophagy remains unknown but a recent meta-analysis estimated the global prevalence of prenatal maternal and postpartum pica to be 27.8% [8]. The African region was reported to have the highest prevalence of over 40% [8]. But these regional and global estimates only reflect the very few studies on the subject and are likely to be an underestimation of the true prevalence.
Considering that geophagy and other forms of pica are common among pregnant women who are among the most vulnerable to environmental exposures, it is essential to understand the health and developmental consequences associated with it. The mystery surrounding geophagy in pregnancy is that even after millennia of persistent practice, very little is understood about its causes and potential consequences for maternal health, immediate birth outcomes and later child health and development. Results from the few published studies on the subject were ambivalent on potential consequences due to mercury poisoning [9], exposure to metals such as cadmium, copper, manganese, arsenic [10, 11], soil-transmitted helminth (STH) infections (A. lumbricoides) [12] and reduced haemoglobin and ferritin concentrations [13].
As a secondary data analysis to the Tovi study, which sought to investigate the impact of prenatal maternal anaemia on early child cognitive development, this paper assesses the relationship between geophagy in pregnancy and maternal anaemia, iron deficiency (ID), malaria and helminth infections, birth outcomes and, in the child, geophagy practices and cognitive and motor development.
Methods
Approximately one year after their children were born, mothers in the Tovi study who had [14] singleton births in Allada, Benin, were asked to respond to a Supplementary Nutrition Questionnaire (SNQ) on their eating habits during pregnancy. The SNQ was initially designed to investigate the sources of high blood lead levels observed in some of the children and mothers and the details are explained elsewhere [15]. As part of the SNQ, mothers responded to questions on geophagy practices during pregnancy and on nutrition and geophageous behaviour of their children. Mothers were asked about consuming processed clay (kalaba or kaolin, both of which are kaolinite soils) or earth during pregnancy, which are three common soil-types consumed by pregnant women in the region. In addition mothers indicated, to the best of their knowledge, in which trimester in pregnancy they practiced geophagy. Women were said to be geophageous if they consumed any of these three soil types during pregnancy. Women were considered to practice polygeophagy if they consumed two or more of these soil types during pregnancy.
Mothers enrolled in this retrospective nutritional survey were HIV-negative and during pregnancy had participated in a clinical trial called Malaria in Pregnancy Preventive Alternative Drugs (MiPPAD) (NCT00811421), which compared the efficacy of two intermittent preventive treatments for malaria in pregnancy (IPTp). The pregnant women were recruited into the clinical trial if they were at most 28 weeks pregnant, HIV-negative and attending antenatal care (ANV) for the first time. Inclusion criteria into the trial included no prior intake of iron, folic acid or vitamin B12 supplements during pregnancy. Detailed inclusion and exclusion criteria for the MiPPAD clinical trial have been published elsewhere [16].
At the first ANV, sociodemographic and anthropometric data, and gravidity of pregnant women were recorded. Pre-pregnancy body mass index (BMI) in kg/m2 was calculated from BMI and gestational age at 1st ANV using the technique presented in an earlier publication [17]. At each of the three visits, blood and stool samples were taken for clinical assessments. Venous blood samples were taken for assessment of haemoglobin (Hb) concentration, serum ferritin concentration and plasmodium parasitemia. Stool samples were taken to determine the presence of helminth eggs using the Kato-Katz technique [18]. C-reactive protein (CRP) concentrations were measured to correct for high ferritin concentrations in participants with inflammations.
During the MiPPAD clinical trial, at the first ANV all women were administered an anthelmintic if they were in the second trimester of pregnancy, following the guidelines of the Beninese Ministry of Health. In addition, throughout pregnancy women were administered daily iron (200 mg oral ferrous sulphate) and folic acid (5 mg daily) supplements until three months after delivery. Women were treated when sick. Iron, folate and medicines for treating illness were provided to pregnant women free of charge. The direct intake of supplements was not monitored.
Anaemia was defined as Hb <110 g/l [19]. Helminth infection was defined as the presence of at least one egg of any intestinal helminth per gram of stool. Iron deficiency was defined as serum ferritin concentration <12μg/l or serum ferritin between 12μg/l and 70 μg/l when CRP concentration was >5mg/L [20].
Gender, weight and gestational age (using fundal height) of the newborn were determined at birth. Low birth weight (LBW) and preterm birth were defined as <2500 g and fewer than 37 weeks of gestation, respectively. At age 1 year, cognitive and motor functions of the children were assessed by a trained nurse using the Mullen Scales of Early Learning (MSEL)[21] adapted for this setting [22]. The MSEL consists of five scales: Gross Motor (GM) scale, Fine Motor (FM) scale, Receptive Language (RL) scale, Expressive Language (EL) scale and Visual Perception (VP) scale. The crude score for each MSEL scale was transformed into normalised scores called the T-scores by using a standardised table with the child’s chronological age at assessment. The age-standardised T-scores of the FM, EL, RL and VP were combined to form the ELC score.
Within three days of the MSEL assessments, a different nurse conducted home visits during which mothers responded to questionnaires on family possessions, the home environment using the Home Observatory Measurement of the Environment (HOME) inventory [23], postnatal depression using Edinburgh Postnatal Depression Scale [24] and maternal postnatal intelligent quotient (IQ) using Raven’s Progressive Matrices test [25]. The second nurse was blind to the MSEL results of the child.
Ethical considerations
Informed consent was sought from all women in the presence of a witness at recruitment into the clinical trial. Illiterate participants provided thumbprints to confirm their consent after after the study had been explained to them in a local language. The Tovi study was approved by the institutional review boards of the University of Abomey-Calavi in Benin and New York University in USA and the Research Institute for Development’s (IRD) Consultative Ethics Committee in France.
Statistical analyses
First we compared and described maternal baseline characteristics during pregnancy and child characteristics at birth between mothers who responded to the SNQ and those who did not respond. We also described the prevalence of geophagy among pregnant women and their offspring. Then we assessed the relationship between mother-child sociodemographic characteristics and geophagy during pregnancy.
Using unconditional logistic regression, we compared the odds of the major maternal outcome variables of interest i.e. anaemia, ID, malaria and helminth infection, at baseline between women who practiced geophagy during the first trimester and those who were not geophageous at the first trimester. Next, since the major maternal outcome variables of interest were assessed repeatedly at different ANVs over the course of pregnancy, mixed-effect models were used to explain the effect of geophagy on the proposed outcomes. Specifically, random intercept was applied at the individual level in all models. Then we compared the model with the random slope at gestational age and random intercept at the individual level to the model with the model with only the random intercept using the likelihood ratio (LR) test. Where the LR test showed significant difference between the models, the model with the random slope was used. Individual-level predictors included in the model were level of education, pre-pregnancy BMI, maternal gestational age, gravidity, age at first ANV, family possession and maternal IQ.
In assessing the consequences of prenatal maternal geophagy on adverse birth outcomes and child development, unconditional logistic regression models were used. For continuous outcomes, multiple linear regressions were used. Stepwise removal of covariates was used to deselect covariates whose P-values were more than 0.05 in the adjusted model with the exception of ID at the period of follow-up.
All statistical analyses were conducted using Stata IC/14.1 (StataCorp Lp, College station, TX).
Results
Of the 828 eligible mothers-child pairs, 552 (66.7%) responded to the SNQ of the Tovi study (Figure 1). Mothers who responded to SNQ had at baseline entry into the clinical trial, lower BMI, lower prevalence of ID, high prevalence of malaria and were more likely to be housewives than non-respondents. Child characteristics at birth were similar among respondent and nonrespondent mothers (Table 1).
Figure 1.
Flowchart of the follow-up of pregnant women and children
Table 1.
Comparison of first ANV maternal baseline characteristics and infant birth outcomes among respondent and non-respondent mothers
| Characteristics | Respondents | Non-respondents | P |
|---|---|---|---|
|
|
|
||
| (n=552) | (n=311) | ||
| Mothers | |||
| Age at 1st ANV (years)a | 25.8 ± 0.3 | 25.9 ± 0.2 | 0.857 |
| Gestational age at 1st ANV (weeks)a | 22.0 ± 0.2 | 22.4 ± 0.2 | 0.145 |
| Prepregnancy BMI (kg/m2)a | 21.0 ± 3.2 | 22.0 ± 4.1 | <0.001 |
| Gravidity | |||
| Primigravida | 100 (18.1) | 55 (17.7) | 0.874 |
| Multigravida | 452 (81.9) | 256 (82.3) | |
| Education | |||
| Primary or more | 177 (32.1) | 112 (36.0) | 0.238 |
| Never schooled | 375 (67.9) | 199 (64.0) | |
| Occupation | |||
| Housewives | 291 (52.7) | 129 (41.5) | 0.002 |
| Employed | 261 (47.3) | 182 (58.5) | |
| Malaria at 1st ANV | |||
| Negative | 456 (82.6) | 275 (88.4) | 0.023 |
| Positive | 96 (17.4) | 36 (11.6) | |
| Anemia at 1st ANV (Hb<110 g/l) | |||
| No anemia | 176 (31.9) | 102 (32.8) | 0.783 |
| Anemia | 376 (68.1) | 209 (67.2) | |
| Iron deficiency at 1st ANV | |||
| No iron deficiency | 386 (69.9) | 190 (61.1) | 0.008 |
| Iron deficiency | 166 (30.1) | 121 (38.9) | |
| Helminth infection at 1st ANV | |||
| Negative | 473 (87.0) | 280 (91.2) | 0.062 |
| Positive | 71 (13.0) | 27 (8.8) | |
| Infants | |||
| Birthweight | |||
| Low (< 2500 g) | 51 (10.0) | 33 (11.4) | 0.542 |
| Normal (≥ 2500 g) | 457 (90.0) | 256 (88.6) | |
| Gestational age at birth | |||
| Preterm (<37 weeks) | 34 (6.3) | 26 (9.0) | 0.149 |
| Normal (≥37 weeks) | 506 (93.7) | 262 (91.0) | |
| Sex | |||
| Boy | 271 (49.1) | 143 (46.0) | 0.379 |
| Girl | 281 (50.9) | 168 (54.0) | |
Unless otherwise stated, values are presented as number (percentage)
Presented as Mean ± SD
ANV- antenatal care visit; BMI-body mass index
The prevalence of geophagy in pregnancy (i.e. geophagy during at least one trimester) was 31.9%. The majority of geophageous pregnant women preferred processed clay (kalaba or kaolin) to earth (Supplementary Table 1). The prevalence of geophagy was highest during the second trimester (21.4%). Forty-five (54.2%) of the geophageous pregnant women at first trimester remained geophageous during second trimester. Polygeophagy was rare among pregnant women and no pregnant woman consumed all three soil-types. About half of one-year-old children were reported to be geophageous by their mothers, of whom 37.6% were geophageous during pregnancy.
There were significantly more housewives than employed women among those who practiced geophagy during the second trimester (Supplementary Table 2). Pregnant women who practiced geophagy during the first trimester were more likely to be anaemic (AOR =1.9, 95%, CI [1.1, 3.4], and less likely to have malaria (AOR = 0.4, 95% CI [0.2, 0.9]) at their first ANV than those who did not (Table 2). Geophagy in pregnancy was not associated with maternal haematological indices, malaria or helminth infections during pregnancy in the multilevel analysis (Table 3).
Table 2.
Prevalence of geophagy and soil preference among pregnant women and infants
| N=552 number (%) |
|
|---|---|
| Mothers | |
| Geophagy (either kalaba or kaolin or earth) | |
| 1st trimester | 83 (15.0) |
| 2nd trimester | 118 (21.4) |
| 3rd trimester | 92 (16.7) |
| Frequency of geophagy | |
| At least once during pregnancy | 176 (31.9) |
| Never during pregnancy | 376 (68.1) |
| Soil preference during pregnancy | |
| Kalaba | 122 (22.1) |
| Kaolin | 55 (10.0) |
| Earth | 18 (3.3) |
| Polygeophagy | |
| Kalaba + kaolin | 18 (3.3) |
| Kalaba + earth | 1 (0.2) |
| Kaolin + earth | 0 (0.0) |
| Kalaba + kaolin + earth | 0 (0.0) |
| Infants | |
| Geophagous | 271 (49.1) |
| Non-geophagous | 281 (50.9) |
Table 3.
Relationship between geophagy in pregnancy and maternal and infant sociodemographic characteristics
| Geophagy at 1st trimester | Geophagy at 2nd trimester | Geophagy at 3rd trimester | |||||||
|---|---|---|---|---|---|---|---|---|---|
|
|
|
|
|||||||
| Yes | No | P | Yes | No | P | Yes | No | P | |
| Age at 1st ANV (years) | 26.1 ± 5.3 | 25.8 ± 5.6 | 0.636 | 25.6 ± 5.6 | 25.9 ± 5.6 | 0.629 | 25.6 ± 5.5 | 25.9 ± 5.6 | 0.632 |
| Gestational age at 1st ANV (weeks) | 21.7 ± 3.9 | 22.0 ± 3.9 | 0.389 | 21.8 ± 4.0 | 22.0 ± 3.8 | 0.492 | 21.7 ± 4.0 | 22.1 ± 3.8 | 0.362 |
| Prepregnancy BMI (kg/m2) | 21.2 ± 2.9 | 21.0 ± 3.2 | 0.649 | 21.2 ± 3.1 | 21.0 ± 3.2 | 0.395 | 21.1 ± 2.8 | 21.0 ± 3.3 | 0.726 |
| Family possession score | 5.8 ± 2.9 | 5.5 ± 2.7 | 0.415 | 5.8 ± 2.8 | 5.5 ± 2.8 | 0.402 | 5.7 ± 2.8 | 5.5 ± 2.8 | 0.537 |
| RAVEN Score | 15.0 ± 3.1 | 15.3 ± 4.9 | 0.991 | 14.4 ± 3.1 | 15.5 ± 5.0 | 0.094 | 14.4 ± 3.3 | 15.5 ± 4.9 | 0.075 |
| EPDS Score | 7.4 ± 4.0 | 8.1 ± 4.1 | 0.200 | 8.4 ± 4.0 | 7.9 ± 4.1 | 0.199 | 8.6 ± 4.1 | 7.9 ± 4.0 | 0.063 |
| HOME Score | 26.9 ± 2.1 | 26.9 ± 2.3 | 0.558 | 27.0 ± 2.1 | 26.8 ± 2.4 | 0.654 | 27.1 ± 2.1 | 26.8 ± 2.3 | 0.303 |
| Gravidity, n (%) | |||||||||
| Primigravida | 12 (12.0) | 88 (88.0) | 0.348 | 23 (23.0) | 77 (77.0) | 0.662 | 18 (18.0) | 82 (82.0) | 0.693 |
| Multigravida | 71 (15.7) | 381 (84.3) | 95 (21.0) | 357 (79.0) | 74 (16.4) | 378 (83.6) | |||
| Education, n (%) | |||||||||
| Primary or more | 25 (14.1) | 152 (85.9) | 0.680 | 50 (28.3) | 127 (71.8) | 0.007 | 37 (20.9) | 140 (79.1) | 0.066 |
| Never schooled | 58 (15.5) | 317 (84.5) | 68 (18.1) | 307 (81.9) | 55 (14.7) | 320 (85.3) | |||
| Occupation, n (%) | |||||||||
| Housewives | 35 (13.4) | 226 (86.6) | 0.311 | 67 (25.7) | 194 (74.3) | 0.020 | 46 (17.6) | 215 (82.4) | 0.567 |
| Employed | 48 (16.5) | 243 (83.5) | 51 (17.5) | 240 (82.5) | 46 (15.8) | 245 (84.2) | |||
Unless otherwise stated, values are presented as Mean ± SD
Presented as number (percentage)
ANV- antenatal care visit; BMI-body mass index; HOME- home observation measurement of the environment; EPDS- Edinburgh postnatal depression scale
As shown in Table 4, children were more likely to be geophageous at age 1 year if their mothers had practiced geophagy at any trimester during pregnancy (P-value<0.05). Children of mothers who practiced geophagy during the third trimester had 3.8 what? [95% CI: 0.6, 6.9] lower GM function at age one year compared to those whose mothers did not practice geophagy during the third trimester in the adjusted model (adjusted for gravidity, maternal education, HOME score, prenatal maternal ID at delivery).
Table 4.
Unconditional logistic regression on the relationship between geophagy at first trimester and maternal health outcomes at baseline
| Iron deficiency | Maternal health outcomes | Helminth | ||
|---|---|---|---|---|
|
| ||||
| Anemia | Malaria | |||
|
|
|
|
|
|
| AOR [95% CI] | AOR [95% CI] | AOR [95% CI] | AOR [95% CI] | |
| Geophagy at 1st trimester | ||||
| Yes | 1.3 [0.8; 2.1] | 1.9 [1.1; 3.4]* | 0.4 [0.2; 0.9]* | 1.0 [0.5; 2.0] |
| No [Reference) | 1 | 1 | 1 | 1 |
AOR- Adjusted odds ratio; ANV-Antenatal care visit
All models were adjusted for gravidity, pre-pregnancy BMI, maternal IQ, gestational age at ANV1, maternal age, family possession, and maternal education
P<0.05
Discussion
We found that pregnant women who practiced geophagy during the first trimester were more likely to be anaemic at their first ANV than women who did not. We did not find differences in later risk of anaemia, or risk of ID, malaria and helminth infection over the course of pregnancy between thee two groups. Geophagy in pregnancy is associated with increased risk of geophagy in children, and if practiced in the third trimester, with poor child gross motor function.
The prevalence of geophagy during pregnancy in this study population is similar to that reported by Mensah et al [26] among pregnant women in Ghana (31.9%). Although geophagy is thought to be a practice common among people of low socioeconomic status, geophagy was not associated with socioeconomic factors of pregnant women in neither the study in Ghana nor in ours. Many other studies also found no association between the prevalence of geophagy and sociodemographic factors [12, 27].
The observed association between prenatal maternal geophagy and increased odds of anaemia and was associated with an increased risk of anaemia at the first ANV as shown by some cross-sectional studies [28, 29]. Although higher odds of ID at first ANV was observed among geophageous pregnant women, the association was not statistically significant. On the contrary, geophagy during the first trimester was associated with reduced odds of malaria at first ANV. A study among the same population in Benin showed that a high iron concentration in pregnancy is associated with an increased risk for malaria and plasmodium parasitaemia.[30] This may explain the reduced likelihood of malaria at first ANV among pregnant women who practiced geophagy during the first trimester although adjusting for ID did not change the strength of the association. We did not find an increased risk of anaemia and iron deficiency in any trimester among geophageous pregnant women, similar to what has been reported in a study with similar longitudinal data [12]. The administration of IFA supplements, IPTp and anthelmintic following the first ANV may have reduced the impact that geophagy in itself had on maternal health outcomes. Daily iron supplementation beginning at first ANV did not attenuate the prevalence of geophagy among pregnant women during the second and third trimesters similar to what was found in randomized control trial in children in Zambia [31]. On the contrary, the prevalence of geophagy was highest during the second trimester with 18% of pregnant women who did not practice geophagy during the first trimester becoming geophageous by the second trimester. In our study population, hookworms were the most prevalent species of soil-transmitted helminths [32]. The most common mode of transmission of hookworms in our population likely is by cutaneous penetration rather than ingestion and this might explain the lack of association observed between geophagy and helminth infection during pregnancy. Pregnant women in Allada, Benin preferred processed and dried clay (kalaba or kaolin) to earth. The processed clay is usually cooked and dried to get rid of moisture and hence less likely to contain helminth eggs than earth.
In terms of birth outcomes and child development, results from our study showed that geophagy, regardless of the trimester, was not associated with preterm birth similar to the findings of a study conducted in Texas [33]. Geophagy at specific trimesters was consistently not associated with increased risk of LBW similar to the results found by some studies that assessed geophagy or pica at only one time during pregnancy [33, 34]. Geophagy at all trimesters of pregnancy was associated with increased risk of geophagy in children. Although the biological mechanism for such an association is unknown, mothers who reported that they practiced geophagy may have been more forthcoming reporting about geophagy practice by their children than those who concealed the practice. Also, children whose mothers practiced geophagy in the third trimester of pregnancy performed poorer on GM scales children of mothers who did not. The biological explanation for this observed relationship is unknown. Even though we have shown in previous research that low prenatal Hb levels are associated with poor GM function of children [14], in the current study prenatal geophagy was not associated with increased risk of anaemia or ID during pregnancy. The observed mean difference in GM scores is approximately 80% of that observed between at-risk autistic and low-risk 14-month-old children [35]. However, this represents 0.38 of the standard deviation of the population mean GM score and thus unlikely to be clinically significant.
The biological significance of geophagy remains controversial even though the practice of geophagy and other forms of pica during pregnancy appears to be common in sub-Saharan Africa. A recent comprehensive review on pica in pregnancy[36] acknowledges the controversy in the findings from published studies. This review attributes the controversy to a number of problems including underreporting, inadequate study design (mainly, cross-sectional), and chanced discovery of geophagy by researchers. These problems inhibit the determination of temporality between geophagy and its risk factors or consequences.
To our knowledge, this study is the first to assess the consequences of prenatal maternal geophagy not only on maternal health and birth outcomes but also on child development and geophagy habits using longitudinal data. Multilevel analysis of the association between geophagy and factors of maternal health allowed us to account for the intra-person variability due to the repeated measurements obtained over the course of pregnancy.
Our study is however limited in the retrospective assessment of geophagy in pregnancy, which could have led to recall bias in the assessment of exposure among respondents. This neither allowed us to assess the quantity and frequency of soil consumption during the period of assessment, nor the physicochemical properties of the type of soil they consumed. Certain types of geophageous clay soils have a therapeutic effect particularly on the skin and the gastrointestinal tract due to their adsorptive properties and their ability to regulate the viscosity and flow of mucus in the intestinal tract [37, 38]. Considering the therapeutic properties of some geophageous soils, the ability to geochemically differentiate between kalaba or kaolin or earth could have added more information to this study. Also, the absence of data on the frequency of consumption did not permit the investigation of potential dose-response relationship between prenatal geophagy and the maternal and child health outcomes considered in this study. Further, maternal baseline characteristics were similar between mothers who responded to the SNQ and those who did not except for BMI, occupation, malaria and iron deficiency; hence we cannot rule out the possibility of non-response bias in this study although it is unlikely that mothers refused participate in the study because of their BMI during their first ANV. Housewives were however easier to find than employed mothers during follow-up data collection.
Conclusion
The findings of our study suggest that women who practice geophagy in pregnancy during the first trimester of pregnancy are more likely to be anaemic at their first ANV. However, geophagy in pregnancy is not associated with increased risk of malaria, helminth, ID or anaemia over the course of pregnancy. Further, geophagy in pregnancy increases the risk of geophagy in children and may lead to poor motor function of infants. Pregnant women should be informed early on about the potential consequences of geophagy during pregnancy.
Supplementary Material
Table 5.
Multilevel models on the consequences of geophagy in pregnancy on maternal health
| Iron deficiency [ID) | Malaria | Anemia | Helminth | |
|---|---|---|---|---|
|
|
|
|
|
|
| AOR [95% CI]a | AOR [95% CI]a | AOR [95% CI]b | AOR [95% CI]a | |
| Geophagy in pregnancy | ||||
| Yes | 1.1 [0.8, 1.6] | 0.6 [0.4, 1.0] | 1.2 [0.7, 1.8] | 0.9 [0.5, 1.6] |
| No [Reference) | 1 | 1 | 1 | 1 |
AOR- Adjusted odds ratio; CI- Confidence interval
Random intercept at the individual level
Random intercept at the individual level and random slope for gestational age.
All models adjusted for maternal gestational age, level of education, pre-pregnancy body mass index, gravidity, family possession score, age at first ANV, and maternal intelligent quotient.
Table 6.
Consequences of geophagy in pregnancy on birth outcomes and infant development
| Geophagy in pregnancy | Birth outcomes | Age one year | |||
|---|---|---|---|---|---|
|
|
|
||||
| Preterm | LBW | Geophagy | ELC score | GM score | |
| AOR [95% CI]b | AOR [95% CI]a | AOR [95% CI]d | AMD [95% CI]h | AMD [95% CI]i | |
| Geophagy during 1st trimester | 1.4 [0.6, 3.6] | 1.7 [0.8, 3.7] | 0.6 [0.4, 1.0]e* | −0.1 [−3.3, 3.2] | 0.4 [−2.8, 3.7] |
| Geophagy during 2nd trimester | 1.0 [0.4, 2.5] | 1.2 [0.6, 2.4]c | 2.8 [1.8, 4.3]f≠ | −0.2 [−3.1, 2.6] | −1.5 [−4.3, 1.4] |
| Geophagy during 3rd trimester | 0.8 [0.3, 2.4] | 1.0 [0.4, 2.3] | 3.0 [1.8, 5.0]e≠ | −2.0 [−5.2, 1.2] | −3.8 [−6.9, −0.6]* |
| Geophagy during at least one trimester | 0.9 [0.4, 2.1] | 1.6 [0.9, 3.1] | 1.5 [1.0, 2.2]g* | −1.1 [−3.6, 1.5] | −1.4 [−3.4, 0.4]j |
AOR- Adjusted odds ratio; CI- Confidence interval; AMD- Adjusted mean difference; LBW- Low birth weight; ELC- Early learning composite; GM- Gross motor; ID – Iron deficiency; BMI - Body mass index
P<0.05;
P<0.001
Adjusted for
gravidity + prenatal ID at time of follow-up,
a + family possession score,
b + ID at 2nd ANV,
pre-pregnancy BMI + maternal IQ + prenatal ID at time of follow-up,
d + maternal education,
a+d+ malaria at 2nd ANV,
a+d+ malaria at 1st ANV,
pre-pregnancy BMI + maternal education + maternal occupation + HOME score+ prenatal ID at time of follow-up,
gravidity + maternal education + HOME score+ prenatal ID at time of follow-up,
i + pre-pregnancy BMI + family possession score
Acknowledgments
We sincerely thank the mothers and children who participated in this study. We also thank the staff of the three health centers (Allada, Attogon, Sékou), Dr. Smaila Ouédraogo, Dr. Manfred Accrombessi, Dr. Ghislain Koura and the entire Tovi and MiPPAD field personnel who were involved in data collection. The Eunice Kennedy Shriver National Institute of Child Health & Human Development (NIH/NICHD) funded The TOVI study, grant R21-HD060524. The MiPPAD trial (NCT00811421-https://clinicaltrials.gov/ct2/show/NCT00811421) was co-funded by the European and Developing Countries Clinical Trials Partnership (EDCTP- IP.07.31080.002). The opinions presented here are the sole responsibility of the authors and do not necessarily represent the views of the funders.
References
- 1.Partnership for Maternal, Newborn & Child Health and WHO. Guide for Implementing Essential Interventions for Reproductive, Maternal, Newborn and Child Health (RMNCH): A Multisectoral Policy Compendium for RMNCH. Geneva: World Health Organisation; 2014. [Google Scholar]
- 2.United Nations. The Millennium Development Goals Report 2015. New York: United Nations; 2015. [Google Scholar]
- 3.Progress towards the Sustainable Development Goals. United Nations; 2017. Report of the Secretary - General E/2017/66. [Google Scholar]
- 4.World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders: Clinical descriptions and diagnostic guidelines. Geneva: World Health Organization; 1992. [Google Scholar]
- 5.Young SL. Pica in Pregnancy: New Ideas About an Old Condition. Annu Rev Nutr. 2010;30:403–422. doi: 10.1146/annurev.nutr.012809.104713. [DOI] [PubMed] [Google Scholar]
- 6.Hippocrates, Littré MPE. Oeuvres complètes d’Hippocrates. Baillière; 1853. [Google Scholar]
- 7.Lin JW, Temple L, Trujillo C, et al. Pica during pregnancy among Mexican-born women: a formative study. Matern Child Nutr. 2015;11:550–558. doi: 10.1111/mcn.12120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Fawcett EJ, Fawcett JM, Mazmanian D. A meta-analysis of the worldwide prevalence of pica during pregnancy and the postpartum period. Int J Gynecol Obstet. 2016;133:277–283. doi: 10.1016/j.ijgo.2015.10.012. [DOI] [PubMed] [Google Scholar]
- 9.Rajaee M, Long RN, Renne EP, et al. Mercury Exposure Assessment and Spatial Distribution in A Ghanaian Small-Scale Gold Mining Community. Int J Environ Res Public Health. 2015;12:10755. doi: 10.3390/ijerph120910755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Nyanza EC, Joseph M, Premji SS, et al. Geophagy practices and the content of chemical elements in the soil eaten by pregnant women in artisanal and small scale gold mining communities in Tanzania. BMC Pregnancy Childbirth. 2014;14:144. doi: 10.1186/1471-2393-14-144. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Kutalek R, Wewalka G, Gundacker C, et al. Geophagy and potential health implications: geohelminths, microbes and heavy metals. Trans R Soc Trop Med Hyg. 2010;104:787–795. doi: 10.1016/j.trstmh.2010.09.002. [DOI] [PubMed] [Google Scholar]
- 12.Kawai K, Saathoff E, Antelman G, et al. Geophagy (Soil-eating) in Relation to Anemia and Helminth Infection among HIV–Infected Pregnant Women in Tanzania. Am J Trop Med Hyg. 2009;80:36–43. [PMC free article] [PubMed] [Google Scholar]
- 13.Geissler PW, Prince RJ, Levene M, et al. Perceptions of soil-eating and anaemia among pregnant women on the Kenyan coast. Soc Sci Med. 1999;48:1069–1079. doi: 10.1016/s0277-9536(98)00409-2. [DOI] [PubMed] [Google Scholar]
- 14.Mireku MO, Davidson LL, Koura GK, et al. Prenatal Hemoglobin Levels and Early Cognitive and Motor Functions of One-Year-Old Children. Pediatrics. 2015 doi: 10.1542/peds.2015-0491. peds.2015–0491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Bodeau-Livinec F, Glorennec P, Cot M, et al. Elevated Blood Lead Levels in Infants and Mothers in Benin and Potential Sources of Exposure. Int J Environ Res Public Health. 2016;13:316. doi: 10.3390/ijerph13030316. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.González R, Desai M, Macete E, et al. Intermittent Preventive Treatment of Malaria in Pregnancy with Mefloquine in HIV-Infected Women Receiving Cotrimoxazole Prophylaxis: A Multicenter Randomized Placebo-Controlled Trial. PLoS Med. 2014;11:e1001735. doi: 10.1371/journal.pmed.1001735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Ouédraogo S, Koura GK, Accrombessi MMK, et al. Maternal anemia at first antenatal visit: prevalence and risk factors in a malaria-endemic area in Benin. Am J Trop Med Hyg. 2012;87:418–424. doi: 10.4269/ajtmh.2012.11-0706. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Tarafder MR, Carabin H, Joseph L, et al. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ‘gold standard’. Int J Parasitol. 2010;40:399–404. doi: 10.1016/j.ijpara.2009.09.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Worldwide prevalence of anaemia 1993–2005: WHO Global database on anaemia. Geneva: World Health Organization; 2008. [Google Scholar]
- 20.Ouédraogo S, Koura GK, Bodeau-Livinec F, et al. Maternal Anemia in Pregnancy: Assessing the Effect of Routine Preventive Measures in a Malaria-Endemic Area. Am J Trop Med Hyg. 2013:12–0195. doi: 10.4269/ajtmh.12-0195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Mullen EM. Mullen Scales of Early Learning: AGS Edition. Circle Pines, Minnesota: American Guidance Service; 1995. [Google Scholar]
- 22.Koura KG, Boivin MJ, Davidson LL, et al. Usefulness of Child Development Assessments for Low-Resource Settings in Francophone Africa. J Dev Behav Pediatr JDBP. doi: 10.1097/DBP.0b013e31829d211c. Epub ahead of print 29 July 2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Caldwell BM, Bradley RH. Home Inventory Administration Manual. University of Arkansas for Medical Sciences; 2001. [Google Scholar]
- 24.Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. Br J Psychiatry J Ment Sci. 1987;150:782–786. doi: 10.1192/bjp.150.6.782. [DOI] [PubMed] [Google Scholar]
- 25.Raven J. The Raven’s Progressive Matrices: Change and Stability over Culture and Time. Cognit Psychol. 2000;41:1–48. doi: 10.1006/cogp.1999.0735. [DOI] [PubMed] [Google Scholar]
- 26.Mensah FO, Twumasi P, Amenawonyo XK, et al. Pica practice among pregnant women in the Kumasi metropolis of Ghana. Int Health. 2010;2:282–286. doi: 10.1016/j.inhe.2010.09.004. [DOI] [PubMed] [Google Scholar]
- 27.Luoba AI, Wenzel Geissler P, Estambale B, et al. Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health. 2005;10:220–227. doi: 10.1111/j.1365-3156.2004.01380.x. [DOI] [PubMed] [Google Scholar]
- 28.Thomson J. Anaemia in pregnant women in eastern Caprivi, Namibia. South Afr Med J Suid-Afr Tydskr Vir Geneeskd. 1997;87:1544–1547. [PubMed] [Google Scholar]
- 29.Young SL, Khalfan SS, Farag TH, et al. Association of Pica with Anemia and Gastrointestinal Distress among Pregnant Women in Zanzibar, Tanzania. Am J Trop Med Hyg. 2010;83:144–151. doi: 10.4269/ajtmh.2010.09-0442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Moya-Alvarez V, Cottrell G, Ouédraogo S, et al. Does Iron Increase the Risk of Malaria in Pregnancy? Open Forum Infect Dis. 2015;2:ofv038. doi: 10.1093/ofid/ofv038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Nchito M, Geissler PW, Mubila L, et al. Effects of iron and multimicronutrient supplementation on geophagy: a two-by-two factorial study among Zambian schoolchildren in Lusaka. Trans R Soc Trop Med Hyg. 2004;98:218–227. doi: 10.1016/s0035-9203(03)00045-2. [DOI] [PubMed] [Google Scholar]
- 32.Mireku MO, Boivin MJ, Davidson LL, et al. Impact of Helminth Infection during Pregnancy on Cognitive and Motor Functions of One-Year-Old Children. PLoS Negl Trop Dis. 2015;9:e0003463. doi: 10.1371/journal.pntd.0003463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Rainville AJ. Pica Practices of Pregnant Women are Associated with Lower Maternal Hemoglobin Level at Delivery. J Am Diet Assoc. 1998;98:293–296. doi: 10.1016/S0002-8223(98)00069-8. [DOI] [PubMed] [Google Scholar]
- 34.Patil CL. Appetite Sensations in Pregnancy among Agropastoral Women in Rural Tanzania. Ecol Food Nutr. 2012;51:431–443. doi: 10.1080/03670244.2012.696012. [DOI] [PubMed] [Google Scholar]
- 35.Ekberg TL, Falck-Ytter T, Bölte S, et al. Reduced Prospective Motor Control in 10-Month-Olds at Risk for Autism Spectrum Disorder. Clin Psychol Sci. 2016;4:129–135. [Google Scholar]
- 36.Young SL. Pica in pregnancy: new ideas about an old condition. Annu Rev Nutr. 2010;30:403–422. doi: 10.1146/annurev.nutr.012809.104713. [DOI] [PubMed] [Google Scholar]
- 37.Williams LB, Haydel SE. Evaluation of the medicinal use of clay minerals as antibacterial agents. Int Geol Rev. 2010;52:745–770. doi: 10.1080/00206811003679737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Droy-Lefaix MT, Tateo F. Chapter 11.6 Clays and Clay Minerals as Drugs. In: Faïza Bergaya BKGT, GL, editors. Developments in Clay Science. Elsevier; pp. 743–752. [DOI] [PMC free article] [PubMed] [Google Scholar]
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