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Keywords:

  • vitamin D deficiency;
  • pregnancy;
  • cord blood;
  • maternal dress cover;
  • maternal diet;
  • dairy products;
  • vitamin supplements

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Halicioglu O, Aksit S, Koc F, Akman SA, Albudak E, Yaprak I, Coker I, Colak A, Ozturk C, Gulec ES. Vitamin D deficiency in pregnant women and their neonates in spring time in western Turkey. Paediatric and Perinatal Epidemiology 2012; 26: 53–60.

Although Turkey is located in a sunny region, vitamin D deficiency is still a serious health problem in pregnant women and their infants, especially among the low socio-economic status Turkish population. This study was carried out in order to measure serum 25-hydroxyvitamin D3 [25(OH)D] concentrations of the pregnant women in the last trimester and in their neonates at delivery and to determine the factors associated with maternal serum 25(OH)D concentrations.

Among the patients visiting the Ege Obstetrics and Gynecology Hospital in the period March to May 2008, 258 healthy pregnant women ≥37 weeks of gestation were included in this study. The information on different characteristics such as the number of pregnancies and births, nutritional status, vitamin and mineral support during gestation, educational status, clothing style and the economic level of the family was collected from women. Blood samples from the mothers and umbilical cord of the newborns were taken to measure 25(OH)D. The mean 25(OH)D concentrations of the mothers and their infants were 11.5 ± 5.4 ng/mL and 11.5 ± 6.8 ng/mL, respectively. We found a strong positive correlation between maternal serum and umbilical cord blood 25(OH)D concentrations (r = 0.651, P < 0.001). The concentration of 25(OH)D was ≤20 ng/mL in 233 mothers (90.3%) and ≤10 ng/mL in 130 mothers (50.4%). Maternal serum 25(OH)D concentrations related strongly to factors such as uncovered dressing style, sufficient consumption of dairy products and multivitamin use during gestation (P < 0.05). About half (52.7%) of these women had a covered dressing style. 25(OH)D concentrations of these covered dressing mothers and their infants were 9.7 ± 5.1 ng/mL and 9.7 ± 5.6 ng/mL, respectively, which were significantly lower compared with those of uncovered mothers and their babies (P < 0.001).

This study showed that, despite a sunny environment, vitamin D deficiency and insufficiency are highly prevalent among the mothers and their neonates. This is generally due to the life style and nutritional status of the mothers. These findings suggest that much more effective vitamin D prophylaxis programmes should be implemented for pregnant women as well as for their babies.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Vitamin D is essential for calcium balance and for the maintenance of bone and muscle health of the body.1 Maternal vitamin D deficiency is a potential threat especially to infants for bone deformities known as rickets, muscle weakness, heart failure, hypocalcaemic convulsions and fetal brain development.2,3 In addition, some studies report that it might be related to type 1 diabetes, asthma, schizophrenia, multiple sclerosis, rheumatoid arthritis, hypertension, cardiovascular heart disease and some cancers in persons of all ages.1,3–5

Major vitamin D sources are sunlight, by triggering cutaneous synthesis in the exposed skin, and some natural foods.1,4 Vitamin D supply of the fetus is provided by placental transfer from the mother, especially in the last trimester of gestation.6 During the first 2 months of life, serum 25-hydroxyvitamin D3 [25(OH)D] concentration of the infants is correlated with that of their mothers, but thereafter, sunlight exposure becomes a major determinant.2,4,7,8 In addition to insufficient maternal vitamin D stores, exclusive breast feeding without vitamin D supplementation also increases the risk of vitamin D deficiency in infants.2,9–11

Several studies have reported a higher risk of vitamin D deficiency in women when pregnant.6,8,12–18 Inadequate consumption of calcium during gestation, ethnically or religiously preferred covered dressing style, dark skin colour, pregnancies in the winter season, air pollution, avoidance of sunlight exposure due to the fear of skin cancer or sunscreen application, lack of vitamin D-fortified foods and lack of vitamin D supplementation during pregnancy have been reported as main factors for maternal vitamin D deficiency.2,9,19

The best indicator of vitamin D status is the serum 25(OH)D concentration, because it is not regulated and reflects both dietary intake from vitamin D and cutaneous synthesis of vitamin D. However, there is no absolute consensus as to what a normal range for 25(OH)D should be. In recent years, as a result of numerous studies, most authors agree that vitamin D deficiency should be defined by a 25(OH)D concentration ≤20 ng/mL (<50 nmol/L) in children and adults.4,20,21 A serum 25(OH)D concentration of 21–29 ng/mL designates vitamin D insufficiency. Moreover, the preferred concentration for 25(OH)D is recommended by many authors to be >30 ng/mL.20,21 The most advantageous serum concentrations for 25(OH)D appeared to be at least 30 ng/mL and those desirable 25(OH)D concentrations for cancer prevention are between 36 and 48 ng/mL.4,22

In the previous studies carried out in Turkey, factors such as insufficient vitamin D supplementation to pregnant women, poor consumption of milk and dairy products, covered dressing style, indoor confinement of women during the day, insufficient exposure to sunlight during winter time have been reported as the main causes of maternal vitamin D deficiency leading to insufficient vitamin D accumulation in the newborn.8,14,16 Although the frequency of vitamin D deficiency has been generally reported to be high in these studies, most of them have been carried out on small groups and there is no study in the Aegean region. So, our aim in the present study was to measure serum 25(OH)D concentrations of pregnant women in the last trimester and in their neonates at delivery and to investigate the demographic and life style factors associated with maternal serum 25(OH)D concentrations in Izmir, the third largest city of Turkey.

Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study design

The study was performed between March and May 2008 in the Ministry of Health Ege Obstetrics and Gynecology Teaching Hospital (located at latitude 38.25°N), which is a tertiary health centre. During the study period, there were 1132 normal vaginal and 1130 caesarean section deliveries. The participants were healthy pregnant women who have been followed-up in this hospital during gestation. All pregnant women who had been pregnant during the winter months and who presented to this hospital for a term delivery in daytime working hours were recruited for the study. We performed our study during spring time (March–April–May) in Izmir (the average temperature of this season is 12–21°C).23 The patient profile of the hospital generally consists of low socio-economic groups. Socio-economic status of the study participants was evaluated according to national poverty level criteria.24

The study was approved by the local ethics committee. Three hundred healthy pregnant women in the last trimester and their healthy infants were enrolled in the study. Written informed consent was obtained from all study subjects. Women with a known history or evidence of rheumatological, thyroid or adrenal diseases, hepatic or renal failure, gestational diabetes, hypertension, pre-eclampsia/eclampsia or any long-term medical therapy were excluded from the study. After delivery, the mothers and their babies who had intrauterine growth retardation (birthweight <2500 g), congenital anomalies or who needed intensive care were also excluded.

Subjects and data collection

A questionnaire with 19 items including demographic characteristics, educational status, annual income, dressing styles of mothers, consumption of milk and dairy products, use of multivitamin supplements during gestation was administered to the pregnant women included in the study. The information about the number of previous pregnancies and births, duration of pregnancy and weight gain during gestation was obtained from medical records. Covered dressing style was defined as covering head and arms but not hands and face with clothes, while the uncovered dressing style was defined as head and arms uncovered. Educational status of each mother was grouped according to the duration of education as follows: 0–5 years (illiterate and primary school graduate), 6–8 years (secondary school graduate), 9 and more (high school and university graduate).

The mothers were asked about frequency and amount of milk and dairy products consumed during gestation. The consumption of dairy products 4–7 days/week of at least 200 mL of milk or its equivalent dairy products such as yoghurt and cheese was regarded as ‘sufficient’ milk consumption, while consumption of dairy products three times a week or less was regarded as ‘insufficient’ milk consumption.25

Sample collection

Maternal blood samples for the measurement of serum 25(OH)D3 were taken within the 3 days before delivery and cord blood samples were taken from neonates at delivery. The sera were separated from all blood samples and stored at −30°C until analysis. Serum 25(OH)D3 concentrations were measured by a chemiluminescence assay using LIASON instrument with the Diasorin kit (Diasorin Inc., Stillwater, MN, USA).

Data analysis

Serum 25(OH)D concentrations <20 ng/mL was classified as deficiency. The vitamin D status of women who had vitamin D deficiency was also classified as:26

  • Mild vitamin D deficiency: Serum 25(OH)D concentration of 10–20 ng/mL (25–50 nmol/L)

  • Moderate/severe vitamin D deficiency: Serum 25(OH)D concentration of <10 ng/mL (<25 nmol/L)

Statistical analysis was performed with SPSS for Windows (version 15.0). Categorical variables were assessed using the chi-squared test. The numeric variables were analysed using Student's t-test and one-way ANOVA. Multiple linear regression analysis was used to determine the association between potential risk factors and maternal serum 25(OH)D3 concentration. Correlation analysis was performed to investigate the relationship between maternal serum and umbilical cord blood 25(OH)D concentrations. A P-value of <0.05 was considered statistically significant.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Characteristics of subjects

A total of 300 mother–infant pairs were enrolled in the study. Forty-two mother–infant pairs were excluded (17 with incomplete questionnaires, 16 with insufficient serum samples and nine mothers who decided to leave the study). The mean age, number of pregnancies and parity of 258 pregnant women in the study were 27.2 ± 4.9 (17–42 age) years, 1.9 ± 1.1 and 0.7 ± 0.7, respectively. Forty-one per cent of the infants were delivered spontaneously and the rest were delivered by caesarean section. Most of the women had been living in the metropolitan area in Izmir and 64% of the mothers had low education status (5 years or less). The majority of the women were unemployed. More than half of the families had an income which was below the national poverty level according to the 2008 data of the Turkish Statistical Agency (i.e. annual income per family <$4100).24 About 52% of mothers used covered-up clothing. Eighty-seven per cent of the women gained normal weight during gestation; 58% had taken multivitamin supplements during the third trimester (one of these women had taken vitamin D and five of them calcium, in addition to multivitamin supplementation) (Table 1).

Table 1.  General characteristics of the mothers in the study
  • a

    Mean ± SD (range).

Age (years)a27.19 ± 4.93 (17–42)
Paritya0.72 ± 0.77 (0–4)
State of employment, n (%) 
 Employed34 (13.2%)
 Unemployed224 (86.8%)
Education, n (%) 
 0–5 years (n = 165)165 (63.9%)
 6–8 years (n = 75)75 (29.1%)
 ≥9 years (n = 18)18 (7.0%)
Weight gain in pregnancy 
 Low (<10 kg)34 (13.2%)
 Normal (10–14 kg)131 (50.8%)
 High (≥15 kg)93 (36.0%)
Consumption of dairy products, n (%) 
 Sufficient146 (56.6%)
 Insufficient112 (43.4%)
Multivitamin use during gestation, n (%) 
 Yes149 (57.8%)
 No109 (42.2%)
Dressing style, n (%) 
 Covered136 (52.7%)
 Uncovered122 (47.3%)

Serum 25(OH)D concentrations

Mean 25(OH)D concentrations were 11.5 ± 5.4 ng/mL in maternal sera and 11.5 ± 6.8 ng/mL in umbilical cord blood. We found a strong positive correlation between maternal serum and umbilical cord 25(OH)D concentrations (r = 0.651, P < 0.001) (Figure 1).

image

Figure 1. The relationship between serum 25-hydroxyvitamin D3 [25(OH)D] concentrations of the mothers and in umbilical cord serum at delivery (solid line shows linear regression).

Download figure to PowerPoint

Serum 25(OH)D concentrations were ≤20 ng/mL in 90.3% and ≤10 ng/mL in 50.4% of the mothers. Severe vitamin D deficiency [25(OH)D ≤5 ng/mL] was detected in 26 (10.1%) mothers. Umbilical cord 25(OH)D concentrations are shown in Table 2.

Table 2.  Vitamin D status [serum 25(OH)D concentrations] of mothers and their infants
Vitamin D statusMothers, n (%)Infants, n (%)
Deficient (≤20 ng/mL)233 (90.3%)233 (90.3%)
 Severe (≤5 ng/mL)26 (10.1%)31 (12.0%)
 Moderate (5–10 ng/mL)104 (40.3%)100 (38.8%)
 Mild (11–20 ng/mL)103 (39.9%)102 (39.5%)
Insufficient (21–29 ng/mL)24 (9.3%)19 (7.4%)
Sufficient (≥30 ng/mL)1 (0.4%)6 (2.3%)

The factors associated with serum 25(OH)D concentrations

In the covered dressing group, mean maternal and umbilical cord 25(OH)D concentrations were both 9.7 ng/mL, compared with 13.5 ng/mL in the uncovered dressing group (P < 0.001) (Table 3).

Table 3.  Mean maternal and umbilical cord serum 25(OH)D concentrations by demographic and life style variables
 Maternal 25(OH)D (mean ± SD) (ng/mL)PUmbilical cord 25(OH)D (mean ± SD) (ng/mL)P
Consumption of dairy products    
 Sufficient (n = 146)13.63 ± 6.18<0.00112.96 ± 6.88<0.001
 Insufficient (n = 112)8.75 ± 4.24 9.59 ± 6.40 
Multivitamin use during gestation    
 Yes (n = 149)12.96 ± 6.29<0.00112.79 ± 7.57<0.001
 No (n = 109)9.52 ± 4.75 9.73 ± 5.32 
Mother's dressing style    
 Covered (n = 136)9.74 ± 5.14<0.0019.73 ± 5.61<0.001
 Uncovered (n = 122)13.48 ± 6.15 13.47 ± 7.60 
Age of mother    
 ≤25 years (n = 102)11.47 ± 5.080.92211.07 ± 6.450.412
 >25 years (n = 156)11.54 ± 6.45 11.79 ± 7.15 
Education    
 0–5 years (n = 165)11.25 ± 5.650.37011.19 ± 6.580.028
 6–8 years (n = 75)11.68 ± 6.3 11.19 ± 6.57 
 ≥9 years (n = 18)13.28 ± 6.82 15.66 ± 9.43 
Annual income    
 <$4500 (n = 126)11.15 ± 5.590.34310.93 ± 6.390.195
 $4500–$9600 (n = 132)11.86 ± 6.25 12.05 ± 7.29 
Parity    
 0–1 (n = 228)11.58 ± 5.790.64511.62 ± 6.990.437
 ≥2 (n = 30)11.04 ± 7.02 10.58 ± 5.95 
State of employment    
 Employed (n = 35)11.87 ± 6.250.70012.32 ± 5.730.451
 Unemployed (n = 223)11.46 ± 5.89 11.38 ± 7.04 
Weight gain during pregnancy    
 Low (<10 kg) (n = 34)10.62 ± 6.480.08210.88 ± 6.870.729
 Normal (10–14 kg) (n = 131)12.33 ± 6.04 11.82 ± 6.38 
 High (≥15 kg) (n = 93)10.69 ± 5.46 11.29 ± 6.87 

The demographic and medical factors relating to serum 25(OH)D concentration of mothers were investigated using multiple regression analysis. This identified three significantly associated factors: dressing style, consumption of dairy products and multivitamin use during gestation (P < 0.05). However, factors such as maternal age, education level, delivery type, weight gain in pregnancy, parity and family income were unrelated to maternal serum 25(OH)D concentrations (Table 4).

Table 4.  Multiple linear regression analysis of factors associated with maternal serum 25(OH)D concentrations (n = 258)
Variablesba (SE)P-valuea
  • R2 = 0.27.

  • b is regression coefficient.

  • a

    All variables are adjusted for one another.

Age of mother−0.001 (0.066)0.989
Education0.130 (0.451)0.773
Annual income−0.123 (0.678)0.856
Weight gain during pregnancy−0.415 (0.501)0.408
Mothers' dressing style3.278 (0.647)<0.0001
Consumption of dairy products3.853 (0.691)<0.0001
Multivitamin use during gestation2.182 (0.696)0.002

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Our findings reveal a high frequency of vitamin D deficiency among pregnant women and their newborns in the spring. The proportions of both mothers and their newborns with serum 25(OH)D concentrations ≤20 ng/mL and ≤10 ng/mL were 90% and 50%, respectively. Cut-off values used to define vitamin D status in non-pregnant adults may not actually reflect vitamin D status in pregnancy. However, because there is no defined cut-off value for 25(OH)D in pregnant women, we used ≤10 ng/mL of serum 25(OH)D concentrations as the indicator of moderate/severe vitamin D deficiency in the statistical analysis as suggested by the literature.27–29 Severe vitamin D deficiency, described as 25(OH)D concentrations <11 ng/mL, has been reported between 46% (autumn) and 80% (spring) in pregnant women and nursing mothers in different regions of Turkey.8,14 However, to our knowledge, the present study surveyed the largest cohort of pregnant women for vitamin D deficiency and is the only study from the Aegean region in Turkey to date.

There are some limitations to our study. One of them is that we could not examine the effects of vitamin D deficiency on bone health and other target organs in the infants. Only 93/258 infants were seen at 3–4 months old. Twenty-eight infants had not received vitamin D supplementation after birth and eight of them had bony changes of rickets in the X-rays. However, no routine biochemistry was available on neonates. Also, the study could not reflect seasonal differences because the study was only conducted in the spring.

We found a strong positive correlation between maternal serum and umbilical cord blood 25(OH)D concentrations in accordance with the literature. Although fetal 25(OH)D concentrations have been reported generally to be lower than maternal concentrations in the literature, maternal and cord blood 25(OH)D concentrations were comparable in the present study.30,31 It is generally considered that maternal vitamin D status is directly responsible for neonatal status.

Vitamin D deficiency in pregnancy is a major risk factor for infants, especially if the pregnant women had not received vitamin D supplementation. In Turkey, it has been reported that the rate of rickets in the 0–3 age group was 6%.32 Appropriate doses of vitamin D supplementation should be given to pregnant women for protection of their babies against rickets in early infancy. Turkish Ministry of Health recommends vitamin D supplementation to pregnant women in the last trimester as 100 000 IU single dose or 1000 IU/day.33 However, in our study group, only one pregnant woman had received vitamin D as recommended. So, the physicians providing antenatal care must pay special attention on this subject to prevent vitamin D deficiency in both the mothers and their infants. Also, inclusion of blood 25(OH)D vitamin D measurement into the neonatal screening programme might be considered in the light of high rates of vitamin D deficiency in pregnant women in Turkey.

In the present study, about half of the mothers had covered dressing style and their serum 25(OH)D concentrations were significantly lower as compared with the uncovered mothers. Mothers with covered dressing style had a threefold risk of low serum 25(OH)D (<11 ng/mL) concentrations as compared with uncovered mothers. Covered dressing style, consumption of dairy products and multivitamin usage during gestation were the statistically significant variables associated with serum 25(OH)D vitamin D concentrations. Our study is in accordance with previous studies showing maternal vitamin D deficiency to be high in mothers with covered dressing style because of their ethnic or religious principles.8,14–18,34–36 In the study of Erol et al.16 carried out in Istanbul in 2005, they found moderate/severe vitamin D deficiency in 70% of 44 pregnant women with covered dressing style. Van der Meer et al.17 measured 25(OH)D concentrations of pregnant non-western women living in the Netherlands and found considerably lower values in the Turkish and Moroccan women; they explained these low results by their dark skin colour, covered dressing style, avoidance of exposure to sunlight and lack of knowledge about the subject.

We found significantly low concentrations of serum 25(OH)D in pregnant women with inadequate intake of milk and milk products compared with women who consumed these products sufficiently. In a study carried out on urban and rural pregnant women in India, serum 25(OH)D concentrations have been shown to be affected by insufficient calcium intake as well as traditional covered dressing style and avoiding going outdoors.15 In various studies it has been shown that calcium and vitamin D are essential elements for bone development from fetal life onwards and that insufficient calcium intake during pregnancy may cause low maternal serum 25(OH)D concentrations. It is therefore highly recommended for pregnant women to have an adequate intake of calcium in order to prevent fetal bone mineral density decrease15,37 by encouraging pregnant women to consume milk and dairy products as well as vitamin D supplements.

In Turkey, in practice, prenatal vitamin supplementation is generally provided as multivitamins containing 200 IU of vitamin D, although daily supplementation at 400 IU/day does not induce adequate serum 25(OH)D concentration during gestation and lactation.38,39 Many experts now agree that in the absence of adequate sun exposure, daily 800–1000 IU vitamin D is needed for children of all ages as well as adults, although this is not the current recommendation of paediatric or governmental organisations.4,40–43 Our findings also showed that although 25(OH)D serum concentrations of the mothers using multivitamins were relatively high as compared with non-users, they were still within the deficiency limits (mean 12.9 ± 6.2 ng/mL). Therefore, as recommended in the literature, daily 1000 IU of vitamin D supplementation should be given to pregnant women at risk of vitamin D deficiency because of their life styles or cultural practices that decrease the time spent outdoors and when clothing covers most of the body surface.7,39,44

In this study, there was no significant association between maternal serum 25(OH)D concentrations and factors such as maternal age, education level, delivery type, weight gain in pregnancy or family income, similar to most other studies,8,13,18 apart from Andiran et al., who found an association between low educational–economic level and vitamin D status of mothers.14

In conclusion, the present study shows that, despite the sunny environment, vitamin D deficiency is highly prevalent among the mothers and their neonates because of the life style and nutritional status of the mothers. These findings suggest that much more efficient vitamin D prophylaxis programmes should be implemented for risk groups such as pregnant women and infants. In addition, food fortification with vitamin D may improve vitamin D status in the population including women of child-bearing age.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This study was supported financially by The Ministry of Health, Tepecik Teaching and Research Hospital, Association of Youth and Sports Club. We thank to all of biochemical laboratory staff for sample collection and testing.

References

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  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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