Abstract
BACKGROUND:
Few studies have been conducted on the prevalence of micronutrient deficiency and its association among pregnant women in South India at different trimesters. Identifying this gap may emphasize the importance of understanding and potentially addressing nutritional deficiencies and anemia risk among pregnant women. The aim was to estimate the prevalence of vitamin D deficiency and anemia and their relationship during the second and third trimesters of pregnancy.
MATERIALS AND METHODS:
A community-based observational study was conducted on pregnant women aged 19–35 years. The study was conducted at a primary health center in the Tiruvallur District of Tamil Nadu from October 2022 to April 2023. Blood samples were collected from the participants during the second trimester and followed up until the third. Hemoglobin levels were measured using photometric cyanmet. Hemoglobin and 25(OH)D3 levels were analyzed using chemiluminescent immunoassay (CLIA). Correlation and linear regression analyses were performed using R software.
RESULTS:
A total of 140 pregnant women participated in this study. The majority of the women were between the ages of 22 and 27 (51.4%) and had an educational level of degree and above (45.0%). The prevalence of anemia in the second trimester was 48.6%, which reduced to 37.9% in the third trimester. In the second trimester, 79.3% of the pregnant women had vitamin D deficiency, which increased to 82.7% in the third trimester. A significant negative association was observed between hemoglobin and vitamin D levels in the second trimester, with a correlation coefficient of –0.31 (95% C.I -0.45, -0.15). However, this was not detected in the third trimester. Univariate and multivariate regression analyses revealed that the vitamin D level in the second trimester was an independent predictor of second-trimester hemoglobin level.
CONCLUSION:
The study findings suggest that many pregnant women experience vitamin D deficiency, particularly during the third trimester. In addition, no significant relationship was found between vitamin D and hemoglobin levels.
Keywords: Hemoglobin, pregnancy trimesters, rural health services, vitamin D
Introduction
Globally, approximately 2 billion people lack essential micronutrients for growth, development, and sustaining health. These micronutrients are integral for fetal weight gain, brain maturation, immune modulation, and musculoskeletal growth and serve as crucial regulators in the development of diverse bodily systems and organs.[1] The micronutrient deficiency is more prevalent in low- and middle-income countries, and this micronutrient deficiency is called hidden hunger.[2] There is limited awareness regarding the significance of a woman’s health and nutritional condition before pregnancy, indicating ample opportunities for enhancing preconception health initiatives at a population scale.[3]
This study focused on two micronutrients, iron and vitamin D, that have been identified during pregnancy. Many studies have revealed that anemia during pregnancy increases the risk of adverse birth outcomes, such as preterm birth, low birth weight, intrauterine growth retardation, and prematurity, particularly in developing regions.[4,5] Similarly, the outcomes for vitamin D deficiency are spontaneous abortion and small-for-gestational-age,[6] gestational diabetes mellitus, hypertensive gestational hypertension, intrauterine growth restriction, stillbirth, and preterm birth.[7,8] In addition, several observational studies have indicated an association between 25(OH)D concentration and hemoglobin status.[9,10] A study stated that a lack of vitamin D potentially worsens iron levels and elevates the likelihood of anemia. The exact reasons for this connection remain unclear, but it is theorized that vitamin D could affect the regulation of iron and the production of red blood cells by affecting hepcidin through cytokines or mechanisms independent of changes in proinflammatory markers. In addition, vitamin D may directly affect the development of red blood cell precursors in the bone marrow.[11]
Anemia poses a significant public health challenge, especially in pregnant and postpartum women. Its prevalence is notably pronounced in low- and lower-middle-income nations, with rural populations and economically disadvantaged households bearing their burdens. The incidence of anemia remains high and affects a substantial proportion of people worldwide. Globally, approximately 37% or 32 million pregnant women aged between 15 and 49 years are affected by anemia.[12] Notably, the National Family Health Survey (NFHS-5) revealed a striking prevalence of 52.2% among pregnant women in India,[13] whereas in Tamil Nadu, the prevalence increased to 62%.[14] Similarly, other factors such as educational attainment, gravidity, and income have traditionally been outlined as iron deficiency anemia determinants of IDA among pregnant women.[15,16] Globally, various reports have shown that 4–60% of pregnant women are affected by vitamin D deficiency. In South India, the prevalence was approximately 42% and 96.3%.[17,18,19] Considering their prevalence, shared risk factors, and diverse effects on similar outcomes, this study examined the relationship in the second and third trimesters of pregnant women in Tamil Nadu.
Materials and Methods
Study design and settings
This prospective observational study was conducted at selected primary health centers in the Tiruvallur district of Tamil Nadu, India. The study was conducted from October 2022 to April 2023.
Study participants and sampling
This study included 140 pregnant women from rural areas who provided written informed consent. The inclusion criteria for participating in the study were women aged between 19 and 35 years at 13–20 weeks of gestation who were willing to participate. Women with comorbidities or unwilling to participate were excluded from the study. Blood samples were collected during the second and third trimesters of pregnancy.
Sample size
This was determined using the following parameters: an expected proportion (p) of 10%, precision (d) of 5%, and a Z value for a 95% confidence interval of 1.96.
The calculated sample size was n = 138, rounded to 140. Therefore, 140 pregnant women were recruited for the study.
Data collection tool and techniques
Following enrollment, participants underwent face-to-face interviews facilitated by a researcher using a standard questionnaire to gather data on demographic profiles, maternal history, and sun exposure habits. In addition, venous blood samples (5 mL) were obtained from each participant at enrollment occurring during the second trimester (between the 13th and 20th gestational weeks). Pregnant women were subsequently monitored for 3 months, during which they received iron supplementation (60 mg twice daily) and calcium supplementation (500 mg + 250 IU of vitamin D). Three months after enrollment (between 25 and 32 weeks of gestational age), another 5 mL venous blood sample was collected for hemoglobin, serum calcium, and plasma concentrations of 25(OH)D3. The sun-exposure questionnaire was administered during the follow-up period.
Variables definition and measurement methods
Anemia in pregnant women is defined by the Indian Council of Medical Research (ICMR) as a hemoglobin level of 11 g/dl or more as normal, 10–10.9 g/dl as mild anemia, 7–9.9 g/dl as moderate anemia, and 4–6.9 g/dl as severe anemia. The Endocrine Society Clinical Practice Guideline defines vitamin D deficiency as serum 25(OH)D levels less than or equal to 20 ng/ml, insufficiency as more than 20 ng/ml but less than 30 ng/ml, and sufficiency or normal as more than or equal to 30 ng/ml. The gestational age was calculated based on the date of enrollment and the date of the first day of the last menstrual period. BMI was calculated as weight in kilograms divided by the square of height in meters. For sun exposure, duration and time were considered. Parity was categorized as 0 and ≥1, and demographic variables were established using the Kuppusamy scale.
Hemoglobin levels were measured using photometric cyanmet hemoglobin, and the results were expressed as g/dl. Stored samples were maintained at temperatures between 2 and 8°C, and the specificity was 1.0, using the cyanmet hemoglobin method. Plasma concentrations of 25(OH)D3 during the second and third trimesters were measured using an electrochemiluminescence binding assay created for Cobas immunoassay analyzers. The results are expressed in ng/mL. For vitamin D, the stored samples were maintained at temperatures between 2 and 8°C. The assay sensitivity for 25(OH)D3 was ± 2.5 ng/mL. Intra-assay precision was demonstrated by coefficient variances (CVs), with a slope ranging from 0.9 to 1.1 and a coefficient of correlation ≥0.95. The bias did not exceed ± 15% at a medical decision threshold of 30 ng/mL for 25(OH)D. Key strategies to control bias in a study include random sampling, standardized measurements, adjustment for confounders, ensuring diverse participant recruitment, and transparent reporting. These measures minimize selection, information, confounding, and sampling and provide the study’s validity and reliability.
Statistical analysis
In this study, the mean ± standard deviation (SD) was used to report continuous variables, while categorical variables were reported as frequencies. To determine the association between the independent variables and the dependent variable hemoglobin levels, Chi-square tests were used. The Pearson correlation coefficient was estimated between hemoglobin and vitamin D levels in the second and third trimesters. Regression analysis was performed to understand the relationship of all demographic and clinical variables, along with vitamin D in the second trimester, with second-trimester hemoglobin. Multivariate analysis was performed with variables that were significant in the univariate analysis. All tests conducted in this study used a significance level of “p < 0.05.” Statistical analysis was performed using R software.
Ethical consideration
The study received Institutional Ethics clearance before initiation (REF: IEC-NI/22/APR/82/52). Subsequently, approval was obtained from the Department of Public Health to conduct the study at the district level. All participants were briefed about the study’s objective and informed that their participation was voluntary. Written informed consent was obtained from all participants before data collection, and confidentiality of all information was ensured.
Results
The study enrolled 140 pregnant women in their second trimester and provided them with supplements until delivery. Most women were aged 18–35 years, housewives, and had a degree. Joint families were more common, nonvegetarian diets were favored, and most had a monthly income ≤ 30,000. Participants’ husbands usually accompanied them. Most pregnancies occurred between the ages of 18 and 23 years, and half of them had their first babies. After routine health talks, sun exposure increased from the second to the third trimester. The prevalence of vitamin D deficiency was high in the third trimester, but hemoglobin levels increased from the second to the third trimester. The frequency distributions of the background variables are listed in Table 1.
Table 1.
Frequency and percentage distribution of background variables (n=140)
| Factor | Frequency (n=140) |
|||||
|---|---|---|---|---|---|---|
| n | % | |||||
| Age in years | ≤22 | 33 | 23.6 | |||
| 23-27 | 72 | 51.4 | ||||
| ≥28 | 35 | 25.0 | ||||
| Educational Qualification | Primary | 4 | 2.9 | |||
| Secondary | 30 | 21.4 | ||||
| Higher Secondary | 35 | 25.0 | ||||
| Diploma | 8 | 5.7 | ||||
| Degree | 63 | 45.0 | ||||
| Mother Occupation | Unemployed | 122 | 87.1 | |||
| Skilled | 4 | 2.9 | ||||
| Professional | 14 | 10.0 | ||||
| Husband education | Primary | 3 | 2.1 | |||
| Secondary | 54 | 38.6 | ||||
| Higher Secondary | 17 | 12.1 | ||||
| Diploma | 20 | 14.3 | ||||
| Degree | 46 | 32.9 | ||||
| Husband occupation | Skilled | 96 | 68.6 | |||
| Professional | 37 | 26.4 | ||||
| Business | 7 | 5.0 | ||||
| Type of family | Joint family | 88 | 62.9 | |||
| Nuclear family | 52 | 37.1 | ||||
| Type of diet | Nonveg | 138 | 98.6 | |||
| Veg | 2 | 1.4 | ||||
| Monthly income | ≤30000 | 115 | 82.1 | |||
| ≤49000 | 7 | 5.0 | ||||
| ≥50000 | 18 | 12.9 | ||||
| Selection of food | Economy | 76 | 54.3 | |||
| Nutrient | 64 | 45.7 | ||||
| Accompanying person | Husband | 118 | 84.3 | |||
| Others | 22 | 15.7 | ||||
| BMI classification | Underweight | 25 | 17.9 | |||
| Normal weight | 60 | 42.9 | ||||
| Overweight | 42 | 30.0 | ||||
| Obesity | 13 | 9.3 | ||||
| Age at marriage | 18-23 | 97 | 69.3 | |||
| 24-29 | 43 | 30.7 | ||||
| Age at menarche | 11-14 | 116 | 82.9 | |||
| 15-18 | 24 | 17.1 | ||||
| Gravida | Primi | 77 | 55.0 | |||
| Multi | 63 | 45.0 | ||||
| Excess menstrual bleeding | Yes | 8 | 5.7 | |||
| Second trimester (sun exposure) | Yes | 3 | 2.1 | |||
| Third trimester (sun exposure) | Yes | 47 | 33.6 | |||
| Gestational age at enrollment, Mean±SD | 15.3±2.3 | |||||
| Second trimester (hemoglobin level), Mean±SD | 10.9±1.1 | |||||
| Second trimester (vitamin D), Median (IQR) | 15.1 (11.6, 19.4) | |||||
| Third trimester (hemoglobin level), Mean±SD | 11.2±1.0 | |||||
| Third trimester (vitamin D), Median (IQR) | 13.5 (10.2, 18.2) | |||||
BMI, body mass index; SD, standard deviation; IQR, interquartile range
According to the guidelines provided by the ICMR, the acceptable level of hemoglobin in the blood is 11 g/dl. During the second trimester, 51.4% of the participants had normal hemoglobin levels, while mild and moderate anemia was present in 30% and 18.6% of the participants, respectively. In the third trimester, 62.1% of the participants had normal hemoglobin levels, while mild and moderate anemia was present in 27.1% and 10.7% of the participants, respectively. Figure 1 shows that after receiving standard care (supplementation), the prevalence of mild and moderate anemia decreased in the third trimester compared with in the second trimester.
Figure 1.
Percentage prevalence of normal hemoglobin level, mild anemia, and moderate anemia in the second and third trimesters of pregnancy
Different reference guidelines exist for categorizing the Vitamin D levels. At a threshold of 20 ng/ml, a small number of participants (n = 4, 2.9%) in the second trimester were within the normal range. The majority were deficient (n = 111, 79.3%), while some had insufficient vitamin D levels (n = 25, 17.9%). In the third trimester, despite receiving standard supplementation, the vitamin D deficiency rate increased to 82.7% [Figure 2].
Figure 2.
Prevalence of vitamin D deficiency, insufficiency, and sufficiency in the second and third trimesters of pregnancy
Table 2 shows the relationship between vitamin D and hemoglobin levels during the second and third trimesters of pregnancy. In the second trimester, there was a significant negative correlation between vitamin D and hemoglobin levels. However, no significant correlation (P = 0.183) was observed during the third trimester.
Table 2.
Correlation between vitamin D and hemoglobin levels in the second and third trimesters of pregnancy
| Time of Measurement | Vitamin D and hemoglobin Correlation |
|||
|---|---|---|---|---|
| Pearson Correlation Coefficient | P | |||
| Second trimester | -0.31 (-0.45, -0.15) | 0.012 | ||
| Third Trimester | 0.11 (-0.27, 0.05) | 0.183 | ||
Linear regression analysis was performed to study the association of different demographic and clinical factors with hemoglobin levels measured in the second trimester [Table 3]. In the univariate analysis, husband’s professional occupation (β = 0.55, P = 0.011) compared to skilled labor and being overweight (β = 0.59, P = 0.037) compared to underweight were linked to higher hemoglobin levels, while higher second-trimester vitamin D levels negatively affected hemoglobin levels (β = -0.05, P < 0.001). In the adjusted analysis, the association of second trimester vitamin D levels remained significant.
Table 3.
Association of various independent variables and vitamin D with hemoglobin levels at second trimester: Unadjusted and Adjusted Analysis
| Parameters | Unadjusted | Adjusted | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
|
|
|
|||||||||
| Beta Hemoglobin (95% CI) | P | Beta Hemoglobin (95% CI) | P | |||||||
| Age in years | ≤22 | Ref | ||||||||
| ≤27 | 0.12 (-0.35,0.59) | 0.611 | ||||||||
| ≥28 | 0.28 (-0.26,0.83) | 0.3 | ||||||||
| Educational Qualification | Primary | Ref | ||||||||
| Secondary | -0.54 (-1.7,0.61) | 0.356 | ||||||||
| Higher Secondary | -0.86 (-2,0.29) | 0.142 | ||||||||
| Diploma | 0.36 (-0.97,1.69) | 0.59 | ||||||||
| Degree | -0.35 (-1.47,0.77) | 0.537 | ||||||||
| Mother Occupation | Unemployed | Ref | ||||||||
| Skilled | 0.51 (-0.63,1.64) | 0.379 | ||||||||
| Professional | -0.21 (-0.84,0.42) | 0.507 | ||||||||
| Husband education | Primary | Ref | ||||||||
| Secondary | 0.44 (-0.85,1.73) | 0.501 | ||||||||
| Higher Secondary | 0.18 (-1.19,1.54) | 0.798 | ||||||||
| Diploma | 0.72 (-0.63,2.07) | 0.292 | ||||||||
| Degree | 0.95 (-0.35,2.25) | 0.15 | ||||||||
| Husband occupation | Skilled | Ref | ||||||||
| Professional | 0.55 (0.13,0.98) | 0.011 | 0.41 (-0.01,0.82) | 0.055 | ||||||
| Business | 0.07 (-0.78,0.93) | 0.864 | 0.02 (-0.81,0.85) | 0.962 | ||||||
| Type of family | Joint family | Ref | ||||||||
| Nuclear family | 0.3 (-0.08,0.69) | 0.123 | ||||||||
| Type of diet | Nonveg | Ref | ||||||||
| Veg | -0.36 (-1.37,0.66) | 0.489 | ||||||||
| Monthly income | ≤30000 | Ref | ||||||||
| ≤49000 | -0.35 (-1.21,0.51) | 0.42 | ||||||||
| ≥50000 | 0.44 (-0.12,1) | 0.124 | ||||||||
| Selection of food | Economy | Ref | ||||||||
| Nutrient | 0.19 (-0.19,0.56) | 0.333 | ||||||||
| Accompanying person | Husband | Ref | ||||||||
| Others | -0.01 (-0.53,0.5) | 0.959 | ||||||||
| BMI classification | Underweight | Ref | ||||||||
| Normal weight | 0.24 (-0.29,0.76) | 0.37 | 0.25 (-0.25,0.75) | 0.333 | ||||||
| Overweight | 0.59 (0.04,1.15) | 0.037 | 0.47 (-0.06,1.01) | 0.082 | ||||||
| Obesity | 0.27 (-0.48,1.03) | 0.477 | 0.23 (-0.49,0.95) | 0.536 | ||||||
| Age at marriage | 18-23 | Ref | ||||||||
| 24-29 | 0.12 (-0.29,0.52) | 0.571 | ||||||||
| Age at menarche | 11-14 | Ref | ||||||||
| 15-18 | -0.04 (-0.54,0.46) | 0.868 | ||||||||
| Gravida | Primi | Ref | ||||||||
| Multi | 0.09 (-0.29,0.46) | 0.651 | ||||||||
| Excess menstrual bleeding | Yes | -0.3 (-1.11,0.51) | 0.464 | |||||||
| No | Ref | |||||||||
| Sun exposure - Second trimester | Yes | 0.41 (-0.89,1.71) | 0.535 | |||||||
| No | Ref | |||||||||
| Vitamin D - Second trimester | -0.05 (-0.08,-0.02) | <0.001 | -0.05 (-0.07,-0.02) | 0.001 | ||||||
The adjusted model includes all the variables significant at a 5% level in the Unadjusted analysis
Discussions
During pregnancy, vitamin D requirements are higher in the second and third trimesters because of an increase in active metabolites, improved calcium absorption, and fetal calcium requirement (250 mg/day in the third trimester), indicating the importance of vitamin D during pregnancy.[20] Likewise, most of the Asian studies have shown that vitamin D deficiency is prevalent among 70–90% of pregnant women during the third trimester, even after supplementation, but these studies did not compare vitamin D levels in the second or first trimester.[21,22,23,24]
In our study, the percentage of pregnant women with vitamin D deficiency increased from 79.3% in second trimester to 82.7% in third trimester after standard care (supplementation). Only a few participants had normal 25(OH)D3 levels (>30 ng/ml). Similarly, a longitudinal study was conducted in Denmark on vitamin D status during pregnancy. The results revealed that vitamin D increased from 16.3% at 18 weeks of gestation to 19.1% at 39 weeks of gestation.[25] A cohort study of maternal serum and breast milk vitamin D levels was conducted in Malaysia. The results revealed vitamin D insufficiency in the second trimester (n = 35), whereas in the third trimester, vitamin D insufficiency increased (n = 41).[26] Similarly, in India, a prevalence study has been conducted on vitamin D deficiency in pregnant women. The study results revealed that vitamin D serum levels were reduced from the first trimester (mean vitamin D = 31.3) to the third trimester (mean vitamin D = 29.1).[27]
In this study, mild and moderate anemia in the second trimester was 30% and 18.6%, respectively. In the third trimester, the prevalence was 27.1% and 10.7%, respectively. After receiving standard care (supplementation), almost 12% of pregnant women could increase their hemoglobin levels from moderate to normal. Similarly, a community-based study was conducted in South India to determine the prevalence of anemia. The study revealed that among antennal women, hemoglobin levels measured at <12 weeks and >25 weeks were 37.7% and 46.6%, respectively.[4] A systematic review and meta-analysis was performed on the prevalence of anemia among pregnant women. A systematic review analyzed 52 studies, and the results revealed that the overall prevalence of anemia in pregnant women was 36.8% (95% CI: 31.5-42.4%). The highest prevalence of anemia was mild at 70.8 (95% CI 58.1-81) and highest in the third trimester of pregnancy, with a prevalence of 48.8 (95% CI 38.7-58.9).[28]
A cross-sectional study was conducted in South Africa on 493 pregnant women aged between 18 and 25 years. This study aimed to investigate the relationship between iron deficiency anemia and vitamin D status. The results showed that anemia and iron deficiency were not significantly related to vitamin D levels of 25(OH)D <20 ng/mL.[29] This study also found a connection between vitamin D and hemoglobin levels during the second and third trimesters of pregnancy. The results revealed that plasma 25(OH)D levels were not significantly associated with Hb concentration in the second trimester. Similarly, a cross-sectional study conducted in Sudan involving 180 pregnant women found no correlation between serum 25(OH)D and Hb levels (r = 0.001, P = 0.999).[30] Two other cross-sectional studies in Bangladesh and Brazil used vitamin D deficiency as an outcome measure and found no association between the two.[31,32] Likewise, a similar cross-sectional study was conducted in South India, and the results showed that there is no association between vitamin D and maternal outcomes.[33] However, in this study, during the third trimester, only a weak positive correlation between vitamin D and hemoglobin levels was observed, which was not statistically significant (P = 0.183). Similarly, a cohort study was conducted in China with a larger sample size of 4419 in the first trimester to the postnatal period 2962 from 2011 to 2018, and the results showed that 25(OH)D was significantly and positively associated with hemoglobin after 32 gestational weeks rather than within 32 gestational weeks.[34] However, in our study, we performed a third-trimester analysis within 32 weeks of gestation. In addition, previous studies have reported that pregnant women with vitamin D deficiency have a significantly higher risk of anemia.[35,36,37,38] In these studies, the reasons for the findings were that they were conducted with a larger sample size. Studies that showed a negative association between 25(OH)D and Hb concentration levels were performed in a smaller sample size. In our study, Table 2 shows specifically that a beta coefficient of –0.05 indicates that for every one-unit increase in vitamin D levels, there is a corresponding decrease of 0.05 units in hemoglobin levels. This suggests that minor fluctuations in vitamin D levels within the range observed in this study may not substantially affect hemoglobin levels. Instead, other factors or interventions may play a more significant role in influencing hemoglobin levels during pregnancy. It is important to note that the supplementation of iron and calcium during pregnancy may influence this relationship, particularly in the third trimester, due to potential interactions between these nutrients and vitamin D. Iron and calcium supplementation can lead to metabolic changes that affect the absorption, utilization, or metabolism of these nutrients, which could alter the association between vitamin D and hemoglobin levels.
Strength
The strength of this study was its prospective design, which involved gathering biochemical and obstetrical variables at different time points throughout pregnancy from the second to the third trimester. This approach allowed a thorough description of the study population. Appropriate analysis was conducted to enhance the credibility of the study findings.
Limitations and recommendations
The main limitation of this study was that it was conducted in only one district, and thus, the findings may not represent the entire country. This means that the findings may have limited generalizability. The study suggests that future research could focus on exploring the mechanisms linking vitamin D deficiency and anemia during pregnancy. This could involve considering factors such as dietary habits, sun exposure, supplementation, and socioeconomic influences in rural settings. It is also recommended to conduct longitudinal studies to understand the impact of these factors on micronutrient deficiency and anemia prevalence, as this could be valuable for developing targeted intervention strategies.
Conclusions
This study aimed to determine whether there is a relationship between plasma 25-hydroxyvitamin D (25(OH)D) and hemoglobin levels in pregnant women. The results showed that there was a negative relationship between plasma 25(OH)D concentration and Hb levels in the second trimester and no relationship in the third trimester. However, the sample size used in the study was not sufficient to draw any conclusions regarding the impact of vitamin D deficiency on hemoglobin levels. Therefore, a more comprehensive study is needed to better understand these associations and develop effective interventions to improve maternal and fetal health outcomes.
Conflicts of interest
There are no conflicts of interest.
Acknowledgment
The researcher is grateful to the study participants and the supervisor for their support and motivation throughout the study, making its successful completion possible.
Funding Statement
Nil.
References
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