Sun Exposure and Vitamin D Supplementation in Relation to Vitamin D Status of Breastfeeding Mothers and Infants in the Global Exploration of Human Milk Study
Adekunle Dawodu 1,* , Barbara Davidson 1, Jessica G. Woo 1, Yong-Mei Peng 2, Guillermo M. Ruiz-Palacios 3, Maria de Lourdes Guerrero 3 and Ardythe L. Morrow 1
1 Global Health Center, Perinatal Institute and Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH 45229, USA
2 Children's Hospital of Fudan University, 399 Wanyuan Road, Shanghai 20102, China
3 National Institute of Medical Sciences and Nutrition, Vasco de Quiroga No. 15, Tlalpan, Mexico City 14000, Mexico
(This article belongs to the Special Issue Nutrition in Pregnancy)
Although vitamin D (vD) deficiency is common in breastfed infants and their mothers during pregnancy and lactation, a standardized global comparison is lacking. We studied the prevalence and risk factors for vD deficiency using a standardized protocol in a cohort of breastfeeding mother-infant pairs, enrolled in the Global Exploration of Human Milk Study, designed to examine longitudinally the effect of environment, diet and culture. Mothers planned to provide breast milk for at least three months post-partum and were enrolled at four weeks postpartum in Shanghai, China (n = 112), Cincinnati, Ohio (n = 119), and Mexico City, Mexico (n = 113). Maternal serum 25(OH)D was measured by radioimmunoassay (<50 nmol/L was categorized as deficient). Serum 25(OH)D was measured in a subset of infants (35 Shanghai, 47 Cincinnati and 45 Mexico City) seen at 26 weeks of age during fall and winter seasons. Data collected prospectively included vD supplementation, season and sun index (sun exposure × body surface area exposed while outdoors). Differences and factors associated with vD deficiency were evaluated using appropriate statistical analysis. vD deficiency in order of magnitude was identified in 62%, 52% and 17% of Mexican, Shanghai and Cincinnati mothers, respectively (p < 0.001). In regression analysis, vD supplementation (p < 0.01), obesity (p = 0.03), season (p = 0.001) and sites (p < 0.001) predicted maternal vD status. vD deficiency in order of magnitude was found in 62%, 28%, and 6% of Mexican, Cincinnati and Shanghai infants, respectively (p < 0.001). Season (p = 0.022), adding formula feeding (p < 0.001) and a higher sun index (p = 0.085) predicted higher infant vD status. vD deficiency appears to be a global problem in mothers and infants, though the prevalence in diverse populations may depend upon sun exposure behaviors and vD supplementation. Greater attention to maternal and infant vD status starting during pregnancy is warranted worldwide.
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In this prospective study of urban population in North America, Latin America and China using the same study design, we found vD deficiency to be common in breastfeeding mothers from Shanghai and Mexico City and less common in mothers in Cincinnati. The mean serum 25(OH)D concentration in lactating mothers in Mexico City (48.2 nmol/L) and in Shanghai (48.6 nmol/L) was lower than the recommended target value of >50 nmol/L . At four weeks postpartum, over 60% of the mothers in Mexico City and half of the mothers in Shanghai were vD deficient ()serum 25(OH)D concentration <50 nmol/L) compared with 17% of mothers in Cincinnati. Most of the vD deficient mothers had moderate vD deficiency (serum 25(OH)D levels of 30 to <50 nmol/L) while 2% of the mothers in Shanghai and Cincinnati and 6.2% of Mexican mothers had severe deficiency (serum 25(OH)D levels <30 nmol/L), which is associated with increased risk of osteomalacia. As expected, there was an inverse relationship between 25(OH)D levels and serum PTH levels, indicating an inadequate vD status in the mothers, which is associated with elevated levels of serum PTH. The degree of severe vD deficiency is significantly lower than previously reported from other countries. Based on previous studies, 61% of breastfeeding mothers from the United Arab Emirates , 48% of mothers in India  and 46% of breastfeeding mothers from Turkey  had severe deficiency (serum 25(OH)D concentration <25 nmol/L), which is associated with increased risk of osteomalacia . Such a low vD status would also predispose breastfeeding infants without vD supplementation to vD deficiency. It thus appears that moderate to severe vD deficiency in early postpartum in breastfeeding mothers is a common problem in many countries and may be under recognized.
In this study, the higher vD status in mothers from Cincinnati was associated with higher sun index and vD supplementation intake compared with mothers in Shanghai and Mexico City. It is of note that the restricted exposure to sunlight during postpartum among Shanghai and Mexican mothers is related to cultural practices in which mothers are restricted from outdoor activities and are cared for by family members. This practice of restricting mothers from outdoor exposure in the immediate postpartum convalescent period (known as “doing the month”) in China has been associated with increased risk of low vD status and rickets in some rural Chinese communities . Recognition of the possible impact of these cultural practices on vD nutrition in postpartum mothers should heighten attention to the need for vD supplementation in such settings. In all of the cohorts from the three sites, vD intake, obesity and season were independent predictors of maternal vD status in multivariate regression analysis. In individual site analysis, high maternal sun index (>500) was associated with high maternal vD status only in the Cincinnati cohort, which attained such a high index. Therefore, differences in the prevalence of these potential risk factors among populations will impact maternal global prevalence, as well as the degree of maternal vD deficiency. For example, in the study from the United Arab Emirates, where severe vD deficiency is more common than in this study, it was found that mothers were more severely sunshine deprived during lactation and had a lower rate of vD supplement intake [28,32].
The vitamin D status of breastfeeding infants who were seen at 26 weeks of age during the fall and winter seasons were lower in the Mexican infants (mean serum 25(OH)D 44 nmol/L) and Cincinnati infants (68.3 nmol/L) than in Shanghai infants (95.3 nmol/L). Vitamin D deficiency, defined as serum 25(OH)D <50 nmol/L, was ten-fold higher in Mexican infants and almost five-fold higher in Cincinnati infants than in Shanghai (62% vs. 28% vs. 6%, respectively). In addition, severe deficiency (serum 25(OH)D <30 nmol/L) was over two-fold higher in Mexican than in Shanghai and Cincinnati infants. This degree of severe deficiency could theoretically predispose Mexican infants to increased risk of rickets [26,27].
Other recent studies indicate that the prevalence of serum 25(OH)D <30 nmol/L is high and variable worldwide in breastfeeding infants, and lack of sun exposure and vD supplementation have been suggested as contributing factors . Twenty-seven percent of breastfeeding infants in Ioannina in Greece , 43%-48% of breastfed infants from New Delhi, India [29,34], and 82% of exclusively breastfed infants in Al Ain, the United Arab Emirates , had serum 25(OH)D <25 nmol/L at 3-6 months of age. It therefore appears that moderate to severe vD deficiency is common in sunshine-deprived and unsupplemented breastfed infants, and reports of clinical rickets may not represent the true picture of low vitamin D status in breastfed infants.
Although the mothers and infants in Shanghai were sunshine deprived in the immediate postpartum period, it is of interest that the infants had a higher sun index than the Cincinnati and Mexican infants during the fall/winter season at 26 weeks of age. Clinical experience also suggested that most (80%) of breastfeeding infants in Shanghai would be on vD supplements, because it is encouraged by care providers . Higher sun index, intake from formula feeding and possible high vD supplementation probably contributed to the higher vD status in Shanghai infants. Using available data from the cohorts from the three sites in the regression analysis, a higher sun index and formula feeding, which increased infant vD intake, were predictors of higher infant vD status at 26 weeks of age. In a previous report, which focused on the Cincinnati site, a shorter duration of exclusive breastfeeding was also predictive of vD sufficiency .
The strength of the study is that we had data to examine the effect of sun exposure and vD supplement intake on maternal vD status at three international sites using the measurement of 25(OH)D levels in a single center. Our study also had a number of limitations. The measurement of 25(OH)D was at only one time point, and we did not have data to compare mother-infant pairs over time. There was lack of information on the vD status of the infants between birth and 26 weeks of age, which could have provided better longitudinal data on the relationship between feeding pattern and serum 25(OH)D concentration in the infant. We did not have blood samples in the infants for comparison of 25(OH)D concentrations during all four seasons across the three sites. We did not evaluate the role of skin pigmentation, which could contribute to vitamin synthesis and serum 25(OH)D levels, especially in Cincinnati cohorts. Additionally, an important limitation was lack of data on the rate of vD supplement intake in the infants at two of the three sites.
The reported vD supplementation rate in infants in the Cincinnati cohort was only 19%. Other studies from the U.S. have also reported a low vD supplementation rate of 5%-19% in breastfeeding infants [36,37], while two recent studies from Canada found high vD supplementation rates of 80%-98%  and 88%-98% in breastfed infants . Advice on vD supplement use from healthcare providers was a positive predictor of supplementation in the Canadian [38,39] and one U.S.  study. In general, breastfed infants rely on transplacental transfer of vD, skin synthesis of vD or vD supplementation. However, due to concern about skin cancer, professional organizations recommend that infants avoid sun exposure . Therefore, if breast milk is a major source of feeding in a setting of low maternal vD status and limited sun exposure, awareness among healthcare providers and caregivers of the need for vD supplement intake should be heightened to prevent vD deficiency in breastfeeding infants.
Vitamin D deficiency is detrimental to the health of mother and infant. From this comparative study using the same study design, it is possible that vD deficiency may be a global health problem in the breastfeeding mother-infant dyad and is related to sun exposure behaviors and vD supplement use between populations. Greater attention to maternal and infant vD status, preferably starting during pregnancy, is warranted worldwide.
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