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Contents: Original Research

Dietary Supplement Use and Its Micronutrient Contribution During Pregnancy and Lactation in the United States

Jun, Shinyoung MPH; Gahche, Jaime J. PhD, MPH; Potischman, Nancy PhD; Dwyer, Johanna T. DSc, RD; Guenther, Patricia M. PhD, RD; Sauder, Katherine A. PhD; Bailey, Regan L. PhD, MPH, RD

Author Information
doi: 10.1097/AOG.0000000000003657

Nutrient requirements increase during pregnancy and lactation, especially for certain micronutrients such as folate, iron, iodine, and copper.1 To prevent possible nutrient inadequacies, clinicians and dietitians routinely recommend or prescribe prenatal supplements. The U.S. Preventive Services Task Force recommends that women who are planning or capable of pregnancy take 400–800 micrograms/day of folic acid,2 and several health organizations recognize the importance of dietary supplements to meet requirements of specific nutrients.3,4 Accordingly, the prevalence of dietary supplement use among pregnant women is substantially higher than that among the general population.5–7 Yet, a recent report on total usual nutrient intakes (from both foods and supplements) among U.S. pregnant women that used data from the National Health and Nutrition Examination Survey (NHANES) 2001–2014 concluded that a significant proportion (more than 10%) of pregnant women are not consuming enough of some nutrients (eg, vitamins A, B6, C, D, and E, folate, calcium, iron, magnesium, and zinc), even though 70% reported the use of dietary supplements.8 Although almost no pregnant women had intakes above the Tolerable Upper Intake Level from food sources alone, dietary supplement use increased the proportion of those with intakes above the Tolerable Upper Intake Level (ie, potentially at risk of adverse effects owing to excessive intakes) of some nutrients, especially iron and folic acid.8

Thus, the use of dietary supplements should be carefully planned to compensate for underconsumed nutrients, as well as to avoid exceeding the Tolerable Upper Intake Level. However, little is known from a national perspective about nutrient-specific supplement use during pregnancy, and even less is known for lactating women. A few previous studies using national data focused on only those supplements containing folic acid, iron, or iodine during pregnancy and lactation.5,7,9,10 Furthermore, although differences in any dietary supplement use by age, family income, and trimester were noted among pregnant women in the NHANES 1999–2006 analysis,5 owing to small sample sizes, stratified analyses by specific types of supplements were not possible. Lastly, the motivations for supplement use (ie, whether based on the recommendation of a health care provider or by the woman's own decision) of pregnant and lactating women have not previously been reported.

The primary aim of the present study was to describe the prevalence of nutrient-specific dietary supplement use and mean daily nutrient intakes from supplements among pregnant and lactating women in the United States, using the NHANES 1999–2014 data. We also examined dietary supplement use by age, family income, and trimester within pregnant women, and motivation for supplement use.

METHODS

The National Health and Nutrition Examination Survey examines a nationally representative, cross-sectional sample of the U.S. civilian, noninstitutionalized population, selected by using a complex, multistage probability design.11 The National Health and Nutrition Examination Survey is conducted by the National Center for Health Statistics, and its protocol was approved by the Research Ethics Review Board at the National Center for Health Statistics; further review for data analysis was not required. Since 1999, NHANES has operated as a continuous survey and includes an in-home interview, in which sociodemographic and dietary supplement use information is collected, followed by a health examination conducted in a mobile examination center within 1–3 weeks, at which pregnancy and lactation information is collected. Survey participants could select English or Spanish as the language of interview or could request a translator. We combined data from the 1999–2014 NHANES for this analysis because the sample size for pregnant and lactating women is very small for each 2-year survey cycle, particularly after 2007; NHANES oversampled pregnant women during 2000–2006 to increase the precision of their estimates.11 The National Center for Health Statistics recommends combining at least 4 years of data to improve the reliability and stability of estimates.12

During the health examination, pregnancy and lactation status was assessed using the reproductive health questionnaire administered by interview on women 12 years and older in tandem with a urinary pregnancy test on women aged 8–59 years. Current pregnancy status was determined based on both self-report and urine pregnancy test results, and lactation status was determined by self-report of currently breastfeeding a child. However, owing to risks of violating anonymity, pregnancy and lactation status is publicly released by NHANES only for women 20–44 years of age since 2007; women of other ages were therefore excluded from this analysis. Women aged 20–49 years had a response rate of 69–81% for the health examination across survey cycles.13 Among women who participated in the mobile examination center examination (n=39,755), we excluded those younger than 20 years (n=18,130), those older than 44 years of age (n=11,910), and those missing dietary supplement use information (n=8). Therefore, the final analytical sample consisted of 9,707 reproductive-aged women categorized as pregnant (n=1,314), lactating (n=297), or nonpregnant and nonlactating women (n=8,096). Women who were concurrently pregnant and lactating (n=26) were included in the lactating group because pregnancy during lactating represents a particularly demanding nutritional condition14 and nutrient requirements for lactating women are higher for most nutrients than for pregnant women.1

During the in-home interview, information on age, sex, race and ethnicity, educational attainment, family income, and marital status was collected through a computer-assisted personal interview. Age was used as a continuous variable or as a categorical variable: 20–34 years and 35–44 years. Self-reported race and ethnicity used in this analysis were as defined in NHANES: non-Hispanic white, non-Hispanic black, Hispanic, and “other race.” According to National Center for Health Statistics analytical guidelines the “other” race category is not presented separately but is included in all other estimates. Educational attainment was categorized as less than high school graduate, high school graduate or equivalent, and some college or higher. The family income-to-poverty ratio was calculated by National Center for Health Statistics as the ratio of annual family income to the poverty guideline to represent family income level. The family income-to-poverty ratio is categorized as 130%, 131–350%, and more than 350%; a family income-to-poverty ratio of 130% is an income eligibility criterion for several federal nutrition assistance programs (eg, Supplemental Nutrition Assistance Program). Marital status was classed as married or living with partner, previously married, or never married. In addition, the trimester of pregnancy (first, second, or third trimester) was coded based on the self-reported month of pregnancy on the reproductive health questionnaire but was available only during 1999–2012. Of the 1,314 pregnant women in these survey cycles, 461 were missing this information, mostly because they did not self-report pregnancy during the questionnaire interview but had positive urinary pregnancy test results.

Dietary supplement data were collected through a 30-day questionnaire in conjunction with a product inventory in the participants' homes. Participants were asked to show the interviewer the containers and labels of any supplements used over the previous 30 days when available, as well as to report type, frequency, duration, and amount taken for each supplement. After data collection, trained nutritionists at National Center for Health Statistics matched the products reported to the NHANES Dietary Supplement Database that contains information on the serving sizes and nutrient contents (according to the product label's supplement facts panel).

We classified dietary supplement products as follows: 1) multi-vitamin-mineral, any product containing three or more vitamins and one or more minerals; 2) single- or multi-vitamin, any product containing at least one vitamin without mineral or botanical ingredient; 3) single- or multi-mineral, any product containing at least one mineral without vitamin or botanical ingredient; 4) botanical, any product with at least one botanical ingredient without vitamin or mineral; and 5) others, such as calcium plus vitamin D and fatty acid products.5,15 In addition, we identified prenatal products according to the formulation type; products were coded as prenatal when the product name stated prenatal or the label indicated that it is for use by pregnant women. From the NHANES 2007–2008 cycle and beyond, for each supplement reported, participants were asked whether they are taking the supplement for their own reasons or because a doctor or health care provider recommended to. Based on this information, we categorized pregnant and lactating women as those who took at least one supplement of any kind or prenatal use based on a health care provider's recommendation and those who took products on their own.

Specific nutrient-containing supplements were categorized based on their ingredients as recommended16; for example, if a product contained folic acid or Metafolin (l-methylfolate), it was identified as folic acid–containing supplements. Mean daily intake of nutrients from each supplement was calculated based on the nutrient amount per serving as stated on the product label, the number of servings consumed as reported by the participant, and the number of days taken in the past 30 days as reported by the participant. A total average daily nutrient intake from individual supplements consumed was summed for each participant. This analysis did not include sodium, potassium, fiber, protein, fats, and carbohydrates because these nutrients are rarely included in dietary supplements.

The population distributions of supplemental nutrient intakes are often skewed,17 so we presented estimated means and medians of nutrient intake from dietary supplements among users in conjunction with the current recommended dietary allowance (RDA), Adequate Intake, and Tolerable Upper Intake Level, established by the Food and Nutrition Board of the Institute of Medicine (now known as the National Academy of Medicine).1 The RDA is the average daily intake level sufficient to meet the nutrient requirement of nearly all healthy individuals in a particular life stage group (eg, pregnant women, lactating women, women aged 19–30 years, and women aged 31–50 years) and, therefore, serves a goal for dietary intake for healthy individuals.18 When the amount of evidence on a nutrient is not enough to set the RDA, an Adequate Intake is set based on estimates of nutrient intake by a group (or groups) of people that are assumed to have Adequate Intakes. The RDA and Adequate Intake are presented here as reference points, but they are not used to estimate the population prevalence of intakes at potential risk for inadequacy. The Tolerable Upper Intake Level is the highest average daily nutrient intake level that is unlikely to pose risk of adverse health effects to almost all individuals.18 Folate is unique in that the unit for the RDA is microgram dietary folate equivalents to take into account the different bioavailability of different folate sources, whereas the Tolerable Upper Intake Level applies only to folic acid, a synthetic form of folate from fortified foods and supplements, but not to food folate.19 Because we examined only folic acid consumed as supplements, we presented the RDA in micrograms of folic acid using the conversion factor of 1 microgram dietary folate equivalent=0.6 micrograms folic acid,19 assuming supplements were consumed with food. This assumption has been made in the most recent Food and Drug Administration guideline for labeling.20

Statistical analyses were performed using SAS 9.3 and SAS-callable SUDAAN 11.1 software. All analyses used survey procedures that account for the complex survey design, incorporating the 16-year examination weights constructed for the combined survey period. Weighting takes into account of the differential probabilities of selection (including oversampling), survey nonresponse, and differences in distributions between final sample and the target population; therefore, using the sampling weights produces nationally representative estimates.12 Standard errors (SEs) were estimated using Taylor Series Linearization. Percentages and SEs of the categorical variables (eg, sociodemographic characteristics and dietary supplement use) and means and SEs of the continuous variables (eg, age and nutrient intake) were examined for pregnant, lactating, and nonpregnant and nonlactating women. Differences in distributions of sociodemographic characteristics among subgroups were assessed using Satterthwaite-adjusted Wald χ2, and a P<.05 was considered statistically significant. Differences in the prevalence of dietary supplement use and mean nutrient intakes among subgroups were assessed using pairwise comparisons, and a Bonferroni-adjusted P<.017 (ie, .05/3 subgroups) was considered statistically significant. Linear trends were tested using orthogonal polynomials; a P<.05 was considered to be statistically significant.

RESULTS

In 1999–2014, pregnant and lactating women tended to be younger than nonpregnant and nonlactating women (P<.017) (Table 1). The majority of pregnant and lactating women were non-Hispanic white, had some college education or higher, and married or living with partner. Seventy-seven percent of pregnant and 70.3% of lactating women used one or more dietary supplements, significantly higher than the 44.8% of nonpregnant and nonlactating women (P<.017). In particular, 64.4% of pregnant and 54.2% of lactating women used a prenatal product, primarily multi-vitamin-minerals, defined as having at least three vitamins and at least one mineral. The prevalence of any supplement use was significantly higher in older pregnant women (88.1%) than in younger pregnant women (75.2%) (P<.05) (Fig. 1). Among pregnant women, both any supplement use and prenatal supplement use increased with increasing income (P<.001) (Fig. 2). During 1999–2012, when trimester information was available, the prevalence of prenatal supplement use was 52.4% among women in the first trimester and increased to 80.0% among those in the second trimester, remaining stable at 80.4% among those in the third trimester (Table 2).

Table 1.
Table 1.:
Sociodemographic Characteristics of and Dietary Supplement Use by Women 20–44 Years of Age by Pregnancy and Lactation Status in the United States, NHANES, 1999–2014
Fig. 1.
Fig. 1.:
Prevalence of dietary supplement use by younger (20–34 years of age) and older (35–44 years of age) pregnant women in the United States, National Health and Nutrition Examination Survey, 1999–2014. *Estimates are significantly different from each other at P<.05.Jun. Dietary Supplements During Pregnancy and Lactation. Obstet Gynecol 2020.
Fig. 2.
Fig. 2.:
Prevalence of dietary supplement use by family income-to-poverty level among pregnant women (20–44 years of age) in the United States, National Health and Nutrition Examination Survey, 1999–2014. *Significant linear trend across family income-to-poverty ratio categories (P<.001).Jun. Dietary Supplements During Pregnancy and Lactation. Obstet Gynecol 2020.
Table 2.
Table 2.:
Prevalence of Dietary Supplement Use by Trimester of Pregnancy Among Pregnant Women 20–44 Years of Age in the United States, NHANES, 1999–2012 (n=790)

During 2007–2014, when NHANES collected the motivations for supplement use, 47.4% of pregnant women took at least one dietary supplement based on a health care provider's recommendation, and 16.1% of pregnant women reported the use based on their own decision (Fig. 3). Similarly, among lactating women, 39.8% took at least one dietary supplement because of a health care provider's recommendation, and 22.8% made the decision on their own. Among nonpregnant and nonlactating women, 11.5% took supplements based on a health care provider's recommendation, 30.6% took on their own.

Fig. 3.
Fig. 3.:
Prevalence of reasons for dietary supplement use among pregnant and lactating women (20–44 years of age) in the United States, National Health and Nutrition Examination Survey, 2007–2014 (n=330). Women who used at least one dietary supplement product based on the recommendation of a health care provider were classed as recommended by a health care provider. Information on the reason for dietary supplement use was available only in 2007–2014.Jun. Dietary Supplements During Pregnancy and Lactation. Obstet Gynecol 2020.

More than 60% of pregnant and lactating women used supplements containing thiamin; riboflavin; niacin; folic acid; vitamins B-6, B-12, C, and D; calcium; iron; selenium; and zinc (Table 3). The prevalence of pregnant and lactating women who took supplements that contained the following nutrients was relatively low: choline (5–8%), iodine (18–20%), magnesium (26–28%), phosphorus (5–6%), and selenium (10–12%).

Table 3.
Table 3.:
Percentages of Women 20–44 Years of Age Using Dietary Supplements Containing Specified Micronutrients by Pregnancy and Lactation Status in the United States, NHANES, 1999–2014

The estimated daily mean intakes of micronutrients from dietary supplements among users are presented in Table 4. Mean intakes of thiamin; riboflavin; niacin; folic acid; vitamins B6, B12, and C, iron; and zinc from supplements alone were at or above their respective RDAs among pregnant and lactating supplement users. In particular, dietary supplements contributed a mean daily intake of 787 micrograms/day of folic acid, 9.2 mg/day of vitamin B6, 10 micrograms/day of vitamin D, 366 mg/day of calcium, 38.4 mg/day of iron, 74.6 mg/day of magnesium and 18.2 mg/day of zinc among pregnant supplement users. Few differences in mean micronutrient intakes among users were observed between pregnant and lactating women. The estimated median intakes from supplements were lower than the means in general, reflecting that the distribution was skewed to the right, but similar patterns by pregnancy and lactation status were observed among median intakes (Appendix 1, available online at http://links.lww.com/AOG/B704).

Table 4.
Table 4.:
Mean Daily Micronutrient Intakes From Dietary Supplements Alone Among Users of Dietary Supplements Containing the Specified Nutrient, by Pregnancy and Lactation Status in the United States, NHANES 1999–2014

Between 1999–2002 and 2011–2014, the prevalence of dietary supplement use remained stable among pregnant and lactating women not only in terms of any supplement used but also in specific product categories and specific nutrient-containing supplement used (Appendix 2, available online at http://links.lww.com/AOG/B704). However, among nonpregnant and nonlactating women, the use of supplements containing iodine (23% in 1999–2002 to 15% in 2011–2014; P<.001) and iron (32% in 1999–2002 to 25% in 2011–2014; P<.001) decreased over time.

DISCUSSION

More than 70% of pregnant and lactating women aged 20–44 years in the United States reported the use of at least one dietary supplement, primarily prenatal supplement. Consistent with previous findings, supplement use was substantially higher among pregnant and lactating women, compared with nonpregnant and nonlactating women.5–7 The majority of pregnant women consumed supplements that contained a wide range of nutrients, with the daily mean intake of selected vitamins and minerals from supplements reaching or exceeding the RDA. The number and amount of nutrients included in prenatal supplements are not standardized, but almost all products contain one or more nutrients at levels that are as much as the RDA or more.21 Therefore, it is important to examine nutrients from supplements, as well as from foods and beverages. Recently, Bailey et al8 estimated the total usual nutrient intakes adjusting for within-person variation from the two 24-hour dietary recalls (including supplements) among pregnant women in the NHANES 2001–2014 and compared those to the dietary reference intakes. A significant number of pregnant women had usual intakes below the Estimated Average Requirements (ie, were at risk of inadequacy) for vitamins A (16%), B6 (11%), C (12%), D (46%), and E (43%); folate (16%); iron (36%); calcium (13%); magnesium (48%); and zinc (11%). Very few met or exceeded the Adequate Intake for choline (8%). The findings of the present study indicate that some of these underconsumed nutrients, namely, magnesium and choline, are not commonly supplemented during pregnancy and lactation, whereas other nutrients (ie, vitamins A, B6, C, D and E; folate; iron; calcium; and zinc) are consumed from supplements by more than 40% of pregnant and lactating women.

Folate is an especially important nutrient during the periconceptional period because it helps the fetus form the neural tube, but it might not be consumed enough from food sources alone.22 Therefore, to help prevent neural tube defects, the U.S. Preventive Services Task Force recommends all women who are planning or capable of pregnancy to take a supplement containing 400–800 micrograms of folic acid each day, emphasizing a month before conception through 2–3 months of pregnancy as the critical period.2 Unfortunately, we found that approximately 30% of pregnant women in their first trimester did not take any folic acid from supplements. Women in their second and third trimesters were more likely to consume any supplement than those in their first trimester, confirming earlier findings by others.5 It may be possible that women in their early pregnancy are not aware of their pregnancy or associated recommendations23 or have difficulties with oral intake owing to pregnancy-related nausea and vomiting.24 Nonetheless, mean daily folic acid intake among users was 787±30 micrograms, which indicates that some users consumed more than recommended amounts; indeed more than 40% of the pregnant supplement users exceeded the Tolerable Upper Intake Level in 2001–2014.8 The Tolerable Upper Intake Level was set based on the exacerbation of the neurologic damage of vitamin B12 deficiency.19 Moreover, the health effects, if any, of high folic acid intake during pregnancy on fetal development remain largely unknown; some data from animal studies and epidemiologic studies raise potential cause for concern, as summarized by Lamers et al.25

For iron, the World Health Organization recommends daily supplementation with 30–60 mg of iron for pregnant women to prevent maternal anemia, puerperal sepsis, preterm birth, and low birth weight throughout pregnancy.26 Specifically for the U.S. population, the Centers for Disease Control and Prevention recommends 30 mg/day of iron supplementation for all pregnant women.27 We found that 72.3% of pregnant women were using iron-containing supplements, which contributed 38.4 mg/day on average among users. This explains the earlier findings of Bailey et al8 that, among pregnant women who took supplements, the prevalence of inadequate iron intake was 80.3% when only food sources were considered, but decreased to 13.9% when dietary supplements were included. At the same time, the prevalence of intakes above the Tolerable Upper Intake Level increased from 0% to 40.2% when including supplements. The Tolerable Upper Intake Level for iron was primarily based on gastrointestinal distress as an adverse effect.28 Among pregnant women who were not using supplements, almost all (95.3%) were at risk of iron inadequacy.8 Lactating women had a similar pattern of iron-containing supplement use as pregnant women.

Iodine plays a critical role in fetal brain development, especially during early pregnancy.28 Information on iodine intake from food sources is not available in NHANES, but an analysis of urinary iodine concentration data from the 2001–2006 NHANES concluded that the iodine status of pregnant women was borderline sufficient; that of lactating women was generally sufficient; and some women, especially those who did not consume dairy products, were at risk for iodine insufficiency based on the World Health Organization criteria.29 To prevent possible insufficiency, the American Thyroid Association recommends that all women who are pregnant, lactating, and planning of pregnancy to supplement 150 micrograms of iodine/day.30,31 Although most prenatal products contain approximately 150 micrograms of iodine,10,21 iodine-containing supplement use very low among pregnant women (20.4% consuming 116 micrograms/day from supplements on average) and lactating women (17.5% consuming 104 micrograms/day from supplements on average) in the United States.7,10,29

Motivations for supplement use have been collected in NHANES since 2007. In 2007–2014, about two-thirds of pregnant and 60% of lactating supplement users took at least one product based on a health care provider's recommendation. These findings were as expected because it is common practice for clinicians and dietitians to recommend or prescribe a prenatal supplement; furthermore, a prescription by a health professional is required for reimbursement by private and public insurance programs. In 1999–2006, 37% and 28% of pregnant women (15–39 years) used prescription and over-the-counter prenatal supplements, respectively.10 Given the wide variety of supplement product formulations available, it is important for health care providers to help individuals review all products they are taking to ensure that safe but not excessive intakes of nutrients are provided.32,33 Women who are not using prenatal supplements may need encouragement, because some barriers to prenatal supplement use have been documented among minority women identified, including adverse effects, forgetting to consume, and perceiving prenatal supplements as unnecessary or ineffective.34 Our results on income differences suggest that limited financial resources may also affect prenatal supplement use among pregnant women.35 Clear and open communication about the benefits of prenatal supplements as well as concerns and alternatives may help improve prenatal supplement use.34

About 9 of 10 pregnant women at 35–44 years of age were using dietary supplements. One possible explanation for the higher prevalence of supplement use in older pregnant women is that they may receive more prenatal and perinatal care, because pregnancy at 35 years or older is associated with a higher risk of complications.36,37 In addition, older pregnant women had higher educational attainment and higher family income and were more likely to be married or living with a partner than their younger counterparts (Appendix 3, available online at http://links.lww.com/AOG/B704), all of which have been previously associated with higher supplement use.5,6

The strengths of this study include statistically reliable estimates of dietary supplement use among pregnant and lactating women in the United States produced by combining eight cycles of NHANES data reflecting 16 years. The National Health and Nutrition Examination Survey collects high-quality data on supplement use by using a 30-day questionnaire along with an in-home inventory in which approximately 80% of all supplement products reported were shown to trained interviewers. The prevalence of supplement use has been largely stable among women of reproductive age during 1999–2014, and the NHANES dietary supplement databases were updated for every survey cycle. However, it should be noted that the number of pregnant women was much smaller in 2007–2014 cycles, compared with 2000–2006 cycles when pregnant women were oversampled, which may have affected the precision of the trend analyses. In addition, the number of lactating women was small even after combining multiple cycles, which contributed to the large SEs and imprecision of estimates. There is a need to further examine supplement use during lactation with a larger sample. Another limitation is that the NHANES database relies on manufacturer's label declarations, which may exceed the label declarations 20% or more.38 Studies supporting the Dietary Supplement Ingredient Database have been chemically analyzing the nutrient contents of dietary supplements, including prenatal supplements. This database should be used to adjust labeled amounts in future research once it's completely developed.38 Little is known about the reporting bias and measurement error structure of dietary supplements.17 Future studies may also examine biomarkers in relation to supplement use.5,10 Lastly, NHANES did not collect information about multiple gestational pregnancies or risk factors, such as history of neural tube defects and MTHFR gene polymorphism, which should be considered when assessing individual's nutritional needs.

In conclusion, the majority of pregnant and lactating women in the United States took at least one dietary supplement at some time during their pregnancy, which contributed many nutrients (eg, thiamin; riboflavin; niacin; folic acid; vitamins B6, B12, and C; iron; and zinc) in doses above the RDAs among users. Although folic acid and iron supplementation is recommended during pregnancy, some supplement users may consume high doses that lead to excessive intakes. However, some of these high doses may be appropriate when they were recommended by health care providers owing to special medical conditions. The use of supplements containing iodine, magnesium, and choline was relatively low among all women of reproductive age, regardless of pregnancy or lactation status. Less than half pregnant and lactating women were taking at least one supplement based on a health care provider's recommendation. Health care professionals should be aware of and communicate information about nutrition and dietary supplement use, especially for folic acid and iron. The American College of Obstetricians and Gynecologists and the American Society for Reproductive Medicine recommend that women who present for prepregnancy counseling should be screened for their diet and supplements to ensure they are meeting the RDAs for essential nutrients.33 However, the lowest prevalence of dietary supplement use remains among women in the first trimester of pregnancy.

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