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Diet quality among pregnant women in the Navajo Birth Cohort Study

Abstract Proper nutrition during pregnancy is vital to maternal health and fetal development and may be challenging for Navajo Nation residents because access to affordable and healthy foods is limited. It has been several decades since reported diet quality during pregnancy was examined on Navajo Nation. We present the first study to estimate iodine intake and use the Healthy Eating Index (HEI‐2015) to assess maternal diet quality among pregnant women in the Navajo Birth Cohort Study (NBCS). Based on dietary intake data derived from food frequency questionnaires, overall estimated micronutrient intake has remained similar since the last assessment in 1981, with potential improvements evident for folate and niacin. A high proportion of women (>50%) had micronutrient intakes from dietary sources below the Estimated Average Requirements during pregnancy. The median urinary iodine concentration for NBCS women (90.8 μg/L; 95% CI [80, 103.5]) was less than adequate and lower than concentrations reported for pregnant women that participated in the National Health and Nutrition Examination Survey (NHANES) between 2011 and 2014. Overall, average diet quality of NBCS women estimated using the HEI‐2015 (62.4; 95% CI [60.7, 64.0]) was similar to that reported for women of child‐bearing age and pregnant women in NHANES. Although, NBCS women had diets high in added sugar, with sugar‐sweetened beverages as the primary contributors. Our study provides updated insights on maternal diet quality that can inform health and nutrition initiatives in Navajo communities emphasizing nutrition education and access to prenatal vitamins and calcium, iodine, and vitamin E dense foods.


| INTRODUCTION
Indigenous communities in the United States have disproportionally higher rates of pregnancy complications, poor birth outcomes, and chronic disease compared with non-Hispanic White women (MacDorman, 2011;MacDorman, Kirmeyer, & Wilson, 2012). These rates are influenced by several community-level factors, including exposure to environmental contaminants, access to prenatal care, socio-economics, and challenging local food environments (HealthyPeople.gov, 2019;Sarche & Spicer, 2008;Vintzileos, Ananth, Smulian, Scorza, & Knuppel, 2002). The tribal lands of the Navajo Nation (Navajo), located in the southwestern United States, encompasses 71,000 km 2 in Arizona, New Mexico, and Utah and is the largest Indian reservation in the U.S. Navajo is sparsely populated, with a large proportion of the population living in rural and geographically remote locations. According to the 2010 U.S. Census, 173,667 people live on the Navajo Nation (90% are Navajo). There is an estimated 10 grocery stores and a total of 84 stores that sell food in the entire Navajo Nation. Access to affordable and healthy foods is low (Kumar et al., 2016;Pardilla, Prasad, Suratkar, & Gittelsohn, 2013), with consequent low reported intakes of fruits and vegetables and high intake of fats in the general population (Ballew et al., 1997;Sharma et al., 2010). On average, it is 15 miles from Navajo chapter houses (seat of local government on the Navajo Nation) to the nearest food store that accepts the Special Supplemental Nutrition Program for Women, Infants, and Children (WIC) and 24 miles to the nearest "healthy" food store (stores with six or more fresh vegetables and fruits). Structural barriers, such as the large distances between grocery stores, income disparities, and lack of access to transportation, foster a challenging food environment on Navajo Nation.
Adequate maternal nutrition is critical for normal fetal development and for reducing the risk of pregnancy complications, such as gestational diabetes (Abu-Saad & Fraser, 2010;Nnam, 2015;Ojha, Fainberg, Sebert, Budge, & Symonds, 2015). More than 30 years has lapsed since the last published study that focused on the dietary intake and micronutrient status of pregnant Navajo women (Butte, Calloway, & Van Duzen, 1981). Butte et al. (1981) found that intake of multiple micronutrients were potentially inadequate based on 24-hr dietary recalls in a small sample of 23 Navajo women. Biochemical assessments in 110 women at or shortly after birth identified about one in five women experiencing anaemia and low serum retinol and a prevalence of low serum zinc concentrations, reflective of population risk for zinc deficiency (Butte et al., 1981).
In 2010, the Navajo Birth Cohort Study (NBCS) was initiated to assess maternal and child health outcomes and address community concerns about uranium exposures in Navajo communities (Hunter, Lewis, Peter, Begay, & Ragin-Wilson, 2015). During the enrolment period (2013)(2014)(2015)(2016)(2017)(2018), the NBCS study team enrolled 781 motherinfant pairs from communities across Navajo Nation. The objective of this analysis was to examine diet quality during pregnancy in a subset of NBCS women using a modified Harvard Service Food Frequency Questionnaire (HSFFQ) that included traditional Navajo foods. With food assistance programs emphasizing healthier foods (Schultz, Byker Shanks, & Houghtaling, 2015) and the inception of Navajo community-based health literacy and food access programs, we hypothesize that maternal diet quality among Navajo women has improved over the last 30 years, but may still reflect constraints imposed by the challenging local food environment.

| Navajo Birth Cohort Study
The sample population for this paper included 781 pregnant Navajo women recruited between February 2013 and June 2018 from locations across the Navajo Nation. Navajo staff recruited women during prenatal visits at participating Indian Health Service or Public Law 638 hospitals on the Navajo Nation. Eligibility was limited to women who had Indian Health Service beneficiary status and (a) a clinically confirmed pregnancy; (b) maternal age between 14 and 45 years; (c) residence on the Navajo Nation for a minimum of 5 years; (d) willingness to deliver at one of six participating Indian Health Service or Public Law 638 hospital facilities; and (e) willingness to allow follow-up evaluations during the baby's first year of life. At time of enrolment, a survey was administered to maternal participants to obtain information about age, employment status, educational attainment, annual household income, and smoking status. Medical records were also reviewed for pre-pregnancy height and weight. A total of 781 women enrolled in NBCS, with 283 completing food frequency questionnaires (FFQs). From these, 41 were excluded due to implausible total energy intake (TEI) of <600 or >5,000 kcal/day, resulting in 242 questionnaires used for dietary intake analysis. Of these individuals, 222 had also completed enrolment surveys to collect demographic and socio-economic information.

Key messages
• Estimated dietary intake of micronutrients in NBCS women improved over the last 30 years, particularly for the B vitamins.
• >50% of NBCS women reported inadequate dietary intakes for several micronutrients, emphasizing the importance of access to and promotion of prenatal multivitamin use for Navajo mothers.
• NBCS women had diets higher in whole grains and fruit intake but also diets higher in added sugar, highlighting the importance of continuing efforts focused on improving the local food environment.
• First study to report iodine status and potential risk of iodine deficiency among Navajo women, emphasizing the need for access to iodine containing multivitamins as a part of women's healthcare.

| Dietary assessment
A modified HSFFQ survey was administered to NBCS women (Baer et al., 2005). The Navajo diet includes native plant-and game-based foods such as dandelion greens, blue corn mush, and mutton (lamb), and transitional foodstuffs such as frybread (deep fried wheat flour), Navajo burgers (fry bread, hamburger patty, and condiments) and Navajo tacos (Kopp, 1986). The NBCS program added these Navajo foods to the HSFFQ instrument based on the guidance from Navajo community members and field staff. FFQ surveys were administered in person by trained women (predominately Navajo) who were either university employees, Navajo Division of Health Community Health representatives, or Indian Health Service employees. Staff were trained using food models and were instructed to use the models while administering the survey. FFQs were administered by trained staff during 36-week prenatal appointments at the hospital or clinic. In some cases, FFQs were administered at the hospital within 1 week of delivery (n = 38; 17%).
Participants were asked about their typical portion size and frequency of consuming each food item (never to six times per day) within the 4 weeks prior to the date of the interview. For the FFQ and other surveys administered, NBCS participants could opt not to answer any question, and this was recorded as "not reported." FFQs were processed, and reported consumption data were converted to nutrient intake by assigning a daily frequency weight and using the Nutrition Data System for Research (NDSR), a computerbased software application developed at the University of Minnesota Nutrition Coordinating Center. The Nutrition Coordinating Center Food and Nutrient Database serves as the source of food composition information used by the NDSR for estimating nutrient intake based on FFQ responses (Schakel, Sievert, & Buzzard, 1988;Sievert, Schakel, & Buzzard, 1989). This database includes over 18,000 foods including 8,000 brand name products. Ingredient choices and preparation methods provide more than 160,000 food variants. Values for 165 nutrients, nutrient ratios, and other food components are generated from the database. The U.S. Department of Agriculture (USDA) Nutrient Data Laboratory is the primary source of nutrient values and nutrient composition in NDSR (Feskanich, Sielaff, Chong, & Buzzard, 1989). Representative recipes for fry bread, blue corn mush, Navajo burger, Navajo taco, and mutton-based foods were added to the database for nutrient determination. Multivitamin supplementation (i.e., prenatal multivitamins) was excluded from our dietary intake analyses.
Pregnancy and age-specific estimated average requirement (EAR) intakes were used as benchmarks to determine intake adequacy and the proportions of participants meeting current recommendations using the EAR cut-point method (Institute of Medicine, 2000). Intake ratios were used as a metric to examine potential changes in nutrient intake between the Butte et al. study and the present study. Mean nutrient intake values were determined for NBCS participants (n = 242), and mean nutrient intake values reported in Butte et al. were used to calculate intake ratios for overlapping nutrients. An intake ratio <1 suggests lower estimated intake, and intake ratios >1 suggest greater estimated intake among NBCS participants compared with the Butte et al. study.

| Diet quality
The Health Eating Index (HEI) is a metric developed to evaluate diet quality (Freedman, Guenther, Krebs-Smith, & Kott, 2008;Miller et al., 2011). The HEI total score is the summation of individual component scores with a maximum total score of 100. Higher scores indicate greater consistency with recommended healthy diet guidelines. We calculated scores for 13 dietary components including total fruit, whole fruit, total vegetables, greens and beans, whole grains, dairy, total protein foods, seafood and plant proteins, fatty acid ratio, refined grains, saturated fat sodium, and added sugar. For the individual components of added sugar, sodium, saturated fat, and refined grains, a low score indicates increased dietary intake of these foods; for all other components, a low score indicates low dietary intake of those foods. We converted NDSR food servings per food group to cup equivalents to conform with HEI-2015 scoring methods. We then calculated a population ratio HEI score for NBCS participants using the method previously outlined (Freedman et al., 2008;Guenther et al., 2014). This method obtains estimates of a population's total intake by taking the sum total of the relevant nutrient and energy across all sampled participants.
Then the ratio of each nutrient to energy is calculated and converted to an HEI score. The total HEI score is the sum of HEI

| Sensitivity analysis
We conducted a sensitivity analysis to investigate how daily prenatal supplements would impact the profile of the study population meeting EAR recommendations. We identified the most commonly consumed prenatal vitamin, as reported by participants, and acquired the reported micronutrient content for this brand. We randomly sampled 5% (N = 11), 25% (N = 56), 50% (N = 111), 75% (N = 167), and 95% (N = 211) of the total study participants (N = 222), for 1,000 iterations, and each time, we added the referred daily supplement values from the prenatal vitamin with the estimated micronutrient intake from the FFQ questionnaire.

| Urinary iodine measurements
Iodine concentrations measured in urine samples collected in the morning, or from other spot urine collections, have been shown to adequately assess a population's iodine status (Rohner et al., 2014).
During a women's 36-week prenatal appointment, trained staff collected spot urine samples (N = 193) in sterile 50-ml urine collection cups pre-screened for metals that were provided by the National Center for Environmental Health's Division of Laboratory Sciences. Urine samples were stored at -80 C until shipped overnight on dry ice to the Division of Laboratory Sciences and, once received, samples were stored at ≤−20 C until preparation for analysis. Urine iodine concentrations were measured using inductively coupled plasma dynamic reaction cell mass spectrometry (Centers for Disease Control and Prevention, 2011).

| Statistical methods
Descriptive statistics for a continuous variable includes sample mean with standard deviation denoted by Mean (SD) and median with the interquartile range denoted by Median (IQR). For hypothesis testing of no difference between groups, the ANOVA and Kruskal-Wallis tests were performed as parametric and non-parametric approaches for robustness of testing conclusion. For categorical variables, frequency and percentage were displayed for each category. The Fisher's exact test was used for testing for associations between stratified groups when count data are presented using a contingency table.
Intakes of added sugars were expressed as contribution (%) to TEI and stratified by age and participation in food assistance programs.
For HEI calculations, we utilized the SAS macros provided by the National Cancer Institute (National Cancer Institute, n.d.). Specifically, the weighted means and variance-covariance matrix were estimated from the dataset and then used for Monte Carlo simulations to generate 10,000 independent observations. The mean of individual HEI components, the total scores, and their confidence intervals were further calculated from the simulated datasets. For NHANES data, the sampling weight was also accounted for. All the statistical analyses were performed using SAS 9.4 (SAS Institute Inc., Cary, NC) or R 3.2.1 (R Development Core Team, Vienna, Austria).

| Human participants statement
All women provided written informed consent for the study protocol approved by the University of New Mexico Institutional Review Board  and the Navajo Nation Human Research Review Board (NNR 11.323). Table 1 presents the characteristics of NBCS women with completed FFQ surveys and enrolment data (N = 222). The mean age for participants was 28.3 ± 6.4 years. The majority of women (74%) reported enrolment in the Special Supplemental Nutrition Program for WIC and the use of prenatal multivitamins, although the frequency of use was not reported. Over half of NBCS women reported an annual household income below $20,000 and had prepregnancy body mass index values characterized as overweight or obese. Overall, the 222 women with completed FFQ surveys lived in communities from across Navajo Nation ( Figure S1). The sociodemographic characteristics for the subset of NBCS women who completed an FFQ survey were comparable with other recent studies on the Navajo Nation (Kumar et al., 2016) and with NBCS women overall (Table 1). No significant differences were observed.

| Mean nutrient intake ratios suggest some improvement in estimated intake over time
Mean intake ratios between Butte et al. (1981) and our study were calculated as a metric to evaluate potential changes in estimated dietary intakes over time ( Figure 1a). Almost all nutrients examined had ratios close to or above one, indicating that estimated micronutrient intake has remained similar or improved slightly over time. Potential improvements were evident for the B vitamins (particularly folate and niacin).

| High proportion of NBCS women have dietary intakes below recommended guidelines
Based on dietary intake alone, a high proportion of NBCS women (>50%) had inadequate intakes of calcium, folate, iron, magnesium, vitamin D, and vitamin E (Figure 1b). The proportion of participants with estimated intakes below the EAR did not differ significantly across subgroups stratified by age, body mass index, education level, household income, and food assistance program participation (Table S4). Vitamin D had the greatest proportion of women with inadequate intakes, followed by vitamin E. A slightly lower proportion of adolescent NBCS women (ages 14-18 years) had inadequate intakes of iron and vitamin D compared with older NBCS women. A high proportion of NBCS women reported prenatal vitamin intake (>90%), however our survey tool limited the ability to collect information on frequency of use. Because a majority of NBCS women reported using a specific brand of prenatal vitamins, we conducted a sensitivity analysis to assess the percentage of NBCS women meeting the EAR for select micronutrients if a given proportion of NBCS women took this brand of prenatal vitamin daily (Figure 1c). This analysis showed a substantial increase in the prevalence of adequate intake for vitamin D, folate, iron, and zinc among NBCS women with daily supplemental intake. The greatest effect of supplementation was on vitamin D, folate, and iron, indicated by the steep slopes for these nutrients (Figure 1c). Supplementation increased the prevalence of calcium and vitamin E adequacy, but to a much lesser extent compared with other nutrients. Even with 95% of NBCS women taking a daily prenatal vitamin, only 40% and 58% of NBCS women would achieve adequate vitamin E and calcium intake, respectively.

| Urinary iodine concentrations indicate less than adequate iodine intake among NBCS women
The median urinary iodine (mUI)

| Overall diet quality for NBCS women is similar to NHANES but differs for some components
Overall, average diet quality of NBCS women based on total HEI scores was similar to that reported for the general population of women of child-bearing age and for pregnant women in NHANES

| Sugar-sweetened beverages are a major contributor to added sugar in the NBCS maternal diet
Sugar-sweetened beverages (SSBs) were the major contributor of added sugar in the diet of NBCS women, followed by sweets and cold cereals ( Figure S2). Sweetened beverages alone contributed 30% of added sugar. The majority of NBCS women reported consuming SSBs, with only 3% indicating no consumption (Table S7).
The median added sugar intake, as a percentage of TEI was 21.9%.
Younger women (<26 years) reported a significantly higher intake of added sugar in their diets (23.4% of TEI), and the contribution of added sugar from fruit/sport beverages (16.7%) was greater compared with older women. Interestingly, dessert foods (sweets) contributed significantly more to added sugar in the diet for older women compared with younger women. Although not statistically significant, the contribution of added sugar from cold cereals was greater among women who reported not participating in food assistance programs.

| DISCUSSION
To inform on-going and new health strategies focused on improving Navajo maternal and fetal health, we evaluated dietary intake of micronutrients and diet quality among NBCS women. Compared with a previous study completed over 30 years ago, estimated micronutrient intake in NBCS women has remained similar or improved slightly, with the greatest gains noted for the B vitamins. This is likely due to folate initiatives and changes in access and intake of enriched and/or fortified foods (Crider, Bailey, & Berry, 2011 iron, magnesium, vitamin D, and vitamin E. These intake estimates, however, do not include any additional intake from prenatal multivitamins. In an effort to expand our policy recommendations, we conducted a sensitivity analysis to assess if adequate intake would increase with daily prenatal vitamin use (Figure 1c). For the majority of micronutrients, including folate, vitamin D, iron, and zinc, regular supplementation is likely to result in a high prevalence of adequate nutrient intake in the current food environment. Access and education regarding prenatal vitamins would be essential for overcoming the majority of nutrient inadequacies. This analysis also revealed that daily supplementation would not increase adequacy for calcium and vitamin E to the same extent as other nutrients, with the prevalence of adequacy remaining <60% for these two nutrients. Efforts focused on nutrition education and access to calcium and vitamin E dense foods would likely be needed to overcome these inadequacies via dietary sources.
The low intake of some nutrients observed in NBCS women may warrant additional attention; this finding should be interpreted with caution, however, because the study design did not emphasize multivitamin intake. In general, the traditional Navajo diet limits dairy and seafood because these items are taboo (Kopp, 1986) and many Navajos are lactose intolerant (Ballew et al., 1997;Newcomer, Thomas, Mcgill, & Hofmann, 1977;Swagerty, Walling, & Klein, 2002). In other populations, these foods are important sources of micronutrients such as iodine, calcium, vitamin D, and others. Routine supplementation of calcium, vitamin D, and DHA/EPA may be prudent for Navajo women of child-bearing age (Kaiser & Campbell, 2014)  Greens and beans 3.1 (2.5-3.7) 3.4 ( used in blue corn-based dishes, is an example of a traditional Navajo food that can serve as a potential source for dietary calcium (Christensen, Sorenson, Hendricks, & Munger, 1998).

| Opportunities to address iodine intake
Dairy and seafood are major sources of iodine. This study is the first to identify the potential for iodine insufficiency among Navajo women. NBCS women had inadequate intake of iodine, with a median urinary iodine concentration <150 μg/L, suggesting a risk of iodine deficiency. Iodine is important for child neurodevelopment and essential for the normal production of thyroid hormones (WHO, 2013).  (Alexander et al., 2017). Our study also highlights knowledge gaps on iodine intake among Navajo women, barriers to taking iodine containing supplements, and Navajo experiences with previous iodine fortification efforts. The New Mexico PRAMS program in partnership with the Navajo PRAMS workgroup monitors health status, behaviours, and experiences of Navajo mothers that reside in New Mexico.
Partnerships with the New Mexico and Navajo PRAMS programs would present opportunities to learn more about promotion and access to iodine containing multivitamins. The PRAMS program is also available in Arizona and Utah, states that extend into Navajo Nation.
Collaboration between the three states on issues related to iodine could provide a comprehensive dataset that can be used to develop evidence-based public health strategies that are feasible and culturally relevant for Navajo communities.

| Overall diet quality
The diet quality of NBCS women, as measured by the HEI-2015, was similar to that estimated for the general population of women of child-bearing age and for a small subset of pregnant women in NHANES. NBCS women had diets lower in refined grains, dairy, and plant protein, slightly higher in fruit and whole grains, and much higher in added sugar compared with the general population of women of child-bearing age in the United States.
Previous studies indicated lower than recommended intakes of fruits and vegetables among Navajo women (Ballew et al., 1997;Sharma et al., 2010), potentially related to fruit and vegetable access issues. However, NBCS women had HEI component scores for whole and total fruit that were both at the maximum score, and the total vegetable score was similar to that for women of child-bearing age and pregnant women in NHANES. A high proportion of NBCS women participate in the WIC program, which encourages intake of fruits, vegetables, and whole grains with the food package that is offered (Schultz et al., 2015). In some settings, changes to the WIC food package over the last 10 years to emphasize these foods have positively influenced the local food environment (Havens,  The FFQ and HEI analyses also enabled evaluation of dietary sodium intake; however, FFQ questionnaires not designed for assessing sodium intake show poor correlation between estimated sodium intake and 24-hr urinary measurements (McLean et al., 2017).
Findings from the present study suggest the NBCS women had diets lower in sodium compared with both representative NHANES populations and previous studies among the Navajo general population that indicated high sodium intake (Basiotis, Lino, & Anand, 1999).
This inconsistency may be explained by our FFQ not appropriately capturing sodium intake. For example, questions about discretionary salt use were not included, which is a common source of measurement error (McLean et al., 2017). Because our FFQ instrument was not designed to assess sodium intake specifically, we recommend additional investigations with a sodium-focused FFQ or 24-hr urinary measurements to understand sodium intake of pregnant Navajo women.
Almost three fourths of the NBCS women reported food assistance program participation; however, the sample size of our study did not allow for us to investigate differences in diet quality based on participation in various food assistance programs. The Federal Distribution Program on Indian Reservations (FDPIR) contributes an estimated 41-60% of the household food supply for an estimated 45% of households, indicating an important potential role for this program in supporting maternal diet quality on Navajo Nation (Pindus et al., 2016). Access to Supplemental Nutrition Assistance Program (SNAP) retailers can be challenging for Navajo Nation residents, and the FDPIR program was designed as a more accessible alternative to SNAP. FDPIR also provides nutrition education activities through small grants for individual nutrition counselling, group cooking demonstrations, and sharing healthy recipes with USDA foods. It is unclear to what extent that NBCS women participate in these activities or others of a similar nature via WIC and Head Start. Engaging tribal and federal stakeholders to integrate findings from this study into current nutrition education and food environment frameworks, such as increasing food access and developing culturally relevant healthy recipes, are key elements of an integrated intervention strategy for improving maternal diet quality (Gittelsohn, Kim, He, & Pardilla, 2013). This study has a number of strengths, including a fairly large sample size and the use of a food frequency questionnaire that can provide important information on the maternal diet (Baer et al., 2005), and was adapted to include food items relevant to the target population. There are also some limitations. The dietary intake data were self-reported and potentially subject to social desirability and recall bias. The response rate for FFQ and socio-demographic information was lower than desired, but is not uncommon given the strained resources commonly found within medically underserved, rural hospitals (Genovesi, Hastings, Edgerton, & Olson, 2014). These challenges are amplified in neonatal units managing birthing complications and competing medical test needs (Vaught & Henderson, 2011). No differences in socio-demographics were observed between the subset of NBCS women that completed FFQ surveys and those that did not, which suggests that this subset is representative of the general NBCS population. Additional biomarkers of micronutrient status were not available, and as a result, we could not estimate the prevalence of maternal micronutrient deficiencies.

| CONCLUSION
This study provides a contemporary portrait of maternal diet quality on Navajo Nation and identifies a continued need for maternal health initiatives focused on creating an environment that promotes a healthy diet and adequate micronutrient intake during pregnancy.