Grains Contribute Shortfall Nutrients and Nutrient Density to Older US Adults: Data from the National Health and Nutrition Examination Survey, 2011–2014

Previous data demonstrate grain foods contribute shortfall nutrients to the diet of U.S. adults. The 2015–2020 Dietary Guidelines for Americans have identified several shortfall nutrients in the U.S. population, including fiber, folate, and iron (women only). Intake of some shortfall nutrients can be even lower in older adults. The present analyses determined the contribution of grain foods for energy and nutrients in older U.S. adults and ranked to all other food sources in the American diet. Analyses of grain food sources were conducted using a 24-hour recall in adults (≥51 years old; n = 4522) using data from the National Health and Nutrition Examination Survey, 2011–2014. All grains provided 278 kcal/day or 14% of all energy in the total diet, ranking as the 4th largest contributor of energy compared to 15 main food groups. All grain foods ranked 1st for thiamin (33%) and niacin (23%) intake relative to 15 main food groups. The grain foods category ranked 2nd highest of 15 main food groups for daily dietary fiber (23%), iron (38%), folate (40%), and magnesium (15%) and was the 3rd largest food group contributor for daily calcium intake (13%). When considering nutrients to limit as outlined by dietary guidance, main group of grains contributed 6% total fat, 5% saturated fat, 14% sodium and 9% added sugar. Breads, rolls and tortillas provided 150 kcal/day or 8% of all energy in the total diet, ranking as the 2nd largest contributor of energy compared to 46 food subcategories. Breads, rolls and tortillas ranked 1st of 46 foods for daily thiamin (16%) and niacin (10%) intake and 2nd for dietary fiber (12%), iron (12%), folate (13%), and magnesium (7%). Breads, rolls and tortillas ranked 3rd largest food group contributor for daily calcium (5%) intake. Ready-to-eat cereals provided 47 kcal/day or 2% of all energy in the total diet, ranking as the 20th largest contributor of energy compared to 46 food subcategories. All ready-to-eat cereals ranked 1st for daily iron (19%), 1st for folate (21%), 5th for dietary fiber (7%), 3rd for niacin (9%), 8th for magnesium (4%), and 13th for calcium (2%) intake. Given all grain foods and specific subcategories of grain foods provided a greater percentage of several underconsumed nutrients than calories (including dietary fiber, iron, and folate), grain foods provide nutrient density in the American diet of the older adult.


Introduction
Food sources of energy and nutrients research in the United States (U.S.) has shown that the grain category can play an important contributory role in the diet of all children, adolescents and adults [1,2]. Specifically, grain foods, relative to energy (kcal) provided a greater percentage of 2015-2020 Dietary Guidelines for Americans (2015-2020 DGA) under-consumed nutrients and nutrients of public health concern [3], including dietary fiber, folate, magnesium, calcium and iron. Breads, rolls, tortillas and

Experimental Section
The NHANES is a nationally-representative, cross-sectional survey of U.S. non-institutionalized, civilian residents. NHANES data are collected by the National Center for Health Statistics of the Centers for Disease Control and Prevention. Written informed consent was obtained for all participants or proxies, and the survey protocol was approved by the Research Ethics Review Board at the National Center for Health Statistics. Data from two NHANES datasets (2011-2012; 2013-2014) were combined for the present analyses in adults ≥51 years old [13]. Nutrient intake data for NHANES 2011-2014 are from the United States Department of Agriculture (USDA) Food and Nutrient Database for Dietary Studies (FNDDS) 5.0 and 6.0 [14]. FNDDS are databases that provide the nutrient values for foods and beverages reported in What We Eat in America (WWEIA), the dietary intake component of NHANES for each data release. The WWEIA Food Categories provide an application to analyze food and beverages as consumed in the American diet. The classification scheme includes 150 unique categories and there are 15 main food groups and 46 subcategories of foods. WWEIA food categories have been previously published by USDA [15].
In the current analyses, each grain food and all other foods reported in WWEIA/NHANES is placed in one of the mutually-exclusive food subcategories by linking each food code contained in FNDDS to one WWEIA category [15]. Mixed grain dishes were separated from the main grains group as a food subcategory, and were included in the current analyses. In the present analyses, the combined NHANES dataset sample included 4522 male and female participants, ≥51 years of age, who had reliable and complete 24-h dietary intake data from WWEIA. Trained individuals complete the 24-h dietary recalls using USDA's dietary data collection instrument, the Automated Multiple-Pass Method, which includes detailed descriptions of all food and amounts consumed by subjects. While two days of 24-h dietary recalls are collected in WWEIA, the current analysis used Day 1 data as this represents the in-person data collection in the Mobile Examination Center [16].

Methods and Statistical Analysis
All statistical analyses were performed using SAS software (Version 9.2, SAS Institute, Cary, NC, USA). SAS PROC SURVEYMEANS was used for all statistical calculations, including means and percentages. Survey weights were used to generate nationally-representative estimates for U.S. adults, which were also adjusted for the complex sample design of NHANES. Mean and standard errors of energy, macronutrients and micronutrients for the daily total diet and from food groups were determined (nutrients from dietary supplements were not considered). Percentages of total energy and nutrient intake contributed from food sources were tabulated by ranked order.

Results
Food sources of energy and nutrients for main food groups are shown in Tables 1-21, which appear in this article. Food sources of energy and nutrients for USDA food subcategories are shown in Supplemental Tables S1-S19 and are available online. All foods are ranked based on energy or nutrient contribution in the total diet. Only values >1.0% contribution to the total diet are reported so as not to consider inconsequential sources.

Main Food Groups: Total Fat, Saturated Fat, Added Sugars and Sodium Contributions
Protein foods, mixed dishes, snacks and sweets were the source for nearly 77% of total fat in the diet (Table 13). Mixed dishes, snacks and sweets, protein foods, milk and dairy, and fats and oils contributed 88% of all saturated fat in the total diet (Table 14). Two main food groups, non-alcoholic beverages, and snacks and sweets contributed nearly 66% of added sugars in the diet ( Table 15). The three largest main food group sources of sodium in the total diet were mixed dishes (29.2%), protein foods (22.7%), and grains (14.1%) ( Table 16).

Subcategory Food Groups: Total Fat, Saturated Fat, Added Sugars and Sodium Contributions
While no one subcategory of food contributed ≥10% of all total fat (Table S11) in the diet, the top ten food sources collectively provided 56.9% of total fat, with fats and oils and sweet bakery products being the largest contributors. Likewise, while fats and oils, and sweet bakery products were the largest contributors of saturated fat (9.5% and 9.2%, respectively), no food item contributed ≥10% of all saturated fat in the diet (Table S12). Two food groups provided nearly half of all added sugars in the total diet (Table S13)-sweetened beverages (25.0%) and sweet bakery products (17.2%). Similar to total fat and saturated fat, there was no food group that provided ≥10% of all sodium in the diet (Table S14). The top ten foods, collectively contributing 53.6% of all sodium in the total diet, were breads, rolls, and tortillas, cured meats/poultry, meat/poultry/fish mixed dishes, soups, grain-based mixed dishes, vegetables (excluding potatoes), poultry, condiments and sauces, sandwiches, and sweet bakery products.

Main Food Groups: Thiamin, Niacin, Riboflavin, Vitamin B6, Vitamin B12
Four main food groups contribute nearly 78% of all thiamin in the diet, with the leading main food group being grain foods, providing 32.6% of thiamin in the total diet (Table 17). For niacin, the top three contributors in the diet were protein foods (29.1%), mixed dishes (22.6%) and grains (22.5%), collectively providing nearly 75% of niacin in the diet (Table 18). The top five contributors of riboflavin, collectively providing 81.2% of riboflavin were non-alcoholic beverages, grains, milk and dairy, protein foods, and mixed dishes (Table 19). Protein foods, grains, mixed dishes and vegetables were the largest contributors of vitamin B6 (72.7%) (Table 20), while protein foods, mixed dishes, milk and dairy, and grains contributed nearly 90% of all vitamin B12 in the diet (Table 21).  Two grain subcategories (i.e., breads, rolls and tortillas, and ready-to-eat cereals) were the largest contributors (≥10% for each food) of thiamin in the diet, collectively providing more than a quarter of thiamin in the total diet (Table S15). Breads, rolls, and tortillas were the only food to provide ≥10% of niacin in the total diet (Table S16). The top two contributors of riboflavin in the total diet were coffee and tea, and milk, collectively providing 23.8% of riboflavin in the diet (Table S17). Ready-to-eat cereals were the sole food subcategory to provide ≥10% of vitamin B6 in the total diet (Table S18), while meats, ready-to-eat cereals, and milk were the top-ranking subcategory of foods for vitamin B12, collectively providing 42.0% of all vitamin B12 in the total diet (Table S19).

Discussion
Americans of all ages are continuously not meeting nutrition recommendations even as previous [8] and current dietary guidelines [3] have identified shortfall and nutrients of public health concern. The current analyses focused on older American adults, as sources of energy and nutrients in this population remain limited. The present analyses determined the contribution of grain foods to energy and nutrients in older U.S. adults and ranked other food sources in the American diet, to provide an assessment of energy and nutrient contribution to the total diet. While all grain foods contributed 14% of all energy in the total diet, ranking as the 4th largest contributor of energy compared to 15 main food groups, grain foods can provide nutrient density to the American diet of older adults given they provide a greater percentage of nutrients than energy to the diet. The grain foods category ranked 2nd highest of 15 main food groups for daily dietary fiber, iron, folate, and magnesium, the 3rd largest main food group contributor for daily calcium intake (13 ± 0.4%) and 1st for thiamin and niacin intake. When evaluating subcategories of foods, breads, rolls and tortillas provided 150 ± 2.8 kcal/day or 8% of all energy in the total diet, ranking as the 2nd largest contributor of energy compared to 46 food subcategories. The grain subcategory of breads, rolls and tortillas ranked 1st of 46 food subcategories for daily thiamin and niacin intake and 2nd for dietary fiber, iron, folate, and magnesium. Breads, rolls and tortillas ranked 3rd largest food subcategory contributor for daily calcium intake. Ready-to-eat cereals provided 47 ± 2.6 kcal/day or 2% of all energy in the total diet, ranking as the 20th largest contributor of energy compared to 46 food subcategories. All ready-to-eat cereals ranked 1st for daily iron, 1st for folate, 5th for dietary fiber, 3rd for niacin, 8th for magnesium, and 13th for calcium intake. When considering nutrients to limit as outlined by dietary guidance, main group of grains contributed 6.27% total fat, 4.58% saturated fat, 14.13% sodium and 8.9% added sugar.
Current and preceding dietary guidance [3,8] for Americans recommend that half of all grains consumed be whole grains, with limitations placed on refined/enriched grain consumption. This may be promoting a perception that non-whole grain foods are not a component of a healthy dietary pattern, due to minimal or less nutrient density and increased caloric intake. The current analysis considered all foods consumed in the American diet, including all grain foods. Additionally, the current analysis did not separate whole-and refined-grain foods, as a key objective included determining the sources of energy and nutrients from all foods, and grain foods in particular, as currently consumed in the older American population. As such, the analysis showed that any perceptions that refined grain foods may be lacking in nutrient density are invalid. Indeed, certain grain foods (i.e., sweet bakery products) in the total diet can contribute nutrients to limit, including added sugar, sodium, and saturated fat and hence, these grain foods should be consumed in moderation and within caloric recommendations as designated by dietary guidance to promote public health. Nonetheless, the entire grain food category is the first, second, or third ranking category delivering dietary fiber, folate, iron, magnesium, calcium, and vitamin D-all nutrients identified as shortfall nutrients by the 2015-2020 DGA [3]. Similarly, further analysis with specific food subcategories within the grain category show that breads, rolls and tortillas, grain foods routinely consumed in the U.S. diet, are also first, second and/or third ranking foods for dietary fiber, folate, calcium, iron, magnesium, vitamin A, for less than 8.5% of all calories and sodium, less than 3% of total fat, less than 2.5% of all saturated fat, and less than 3.5% of all added sugar in the total diet. Comparably, the current data provide sources of energy and nutrients data in the older American adult for ready-to-eat cereals, another commonly consumed grain food in the U.S. Ready-to-eat cereals are first, second, third, fourth, and/or fifth ranking foods for dietary fiber, folate, iron, vitamin A, vitamin D for less than 2.5% of all calories and sodium, less than 1% of total fat, less than 0.5% of all saturated fat, and less than 4% of all added sugar in the total diet.
Many older Americans are not meeting recommendations for several key nutrients, many of which are contributed by grain food products. Thus, maintaining both whole-and refined/enriched grains, as part of a healthy dietary pattern, may prove to benefit nutrient intakes in a substantial portion of the U.S. older population. The 2015-2020 DGAs identified shortfall nutrients in all Americans 2 years of age, however, intake of shortfall nutrients can be even lower in older adults. A recent NHANES analysis examining food and supplement use in various age groups found significant differences in the proportion of the population with intakes below EAR. Adults ≥71 years of age had a higher prevalence of inadequacy for calcium, magnesium, and most B vitamins compared to middle-aged and younger adults. Overall, when considering food consumption alone, the data showed that older adults had lower intake and higher prevalence of inadequacy for most nutrients relative to younger adults, with use of dietary supplements being associated with the greatest benefit in older adults [12]. An Irish cross-sectional analysis that explored dietary intakes of community-dwelling elderly individuals found that a substantial number of participants had inadequate intakes of several nutrients, including calcium, magnesium, vitamin D, folate, zinc and vitamin C [17]. U.S. national surveys of dietary intake consistently report all Americans, including older adults, do not meet recommendations for dietary fiber intake [18]. A review by Allen (2009) reported that in the U.S. and the United Kingdom, approximately 6% of adults ≥60 years of age are vitamin B12 deficient, with prevalence of deficiency increasing as individuals age [19]. Another cross-sectional study of free-living New York city older adults participating in the Cardiovascular Health of Seniors and Built Environment Study, found that both genders fell short on recommended intake for fiber, calcium, magnesium, potassium, zinc, folate, and vitamins A, B6, C, D, and E, and in some instances, women had intakes for thiamin below the recommendations [20]. Similarly, a recent systematic review identified inadequate intake of vitamin D, thiamin, riboflavin, calcium, magnesium, and selenium in community-dwelling older adults from North America, Europe, Australia and New Zealand [21] population.
The current analyses have a limitation inherent in observational research and has previously been reported in similar research designs. The results are dependent on self-reported dietary data for foods, which may involve study participants under-or over-estimating food consumption, leading to inaccuracies in energy and nutrient intakes. Data were also obtained using a 24-hour dietary recall, which relies on study participant memory, and while validated methods are used to gather the data, recall information is subject to inaccuracies and bias from memory challenges and other potential measurement errors experienced in epidemiological investigations [22]. Caution should be administered when comparing the current findings to previous studies, as food groupings can impact sources of energy and nutrient outcomes, specifically where there are differences in the level of aggregation (i.e., the number of food groups) or disaggregation methods used by researchers. A significant benefit of using NHANES data for the current analyses includes access to a large and nationally-representative dataset of adults of various age groups in the U.S. and corresponding food and nutrient intake data.

Conclusions
Although existing dietary guidance recommends an increase in shortfall nutrients and nutrients of public health concern, predominantly through food consumption, gaps in nutrient intakes persist in older U.S. adults. The current sources of energy and nutrients analyses show that cumulatively, a variety of grain foods, regularly consumed by older American adults, in addition to other nutrient-dense foods, including fruits and vegetables, help contribute to nutrient density in the total diet. Specifically, grain foods are contributors (≥10% in the total diet) of the 2015-2020 DGA under-consumed shortfall nutrients and nutrients of public health concern, including dietary fiber, folate, magnesium, calcium and iron, vitamin A, vitamin E, vitamin B12, niacin, and thiamin. The subcategory of breads, rolls and tortillas are contributors of daily thiamin, niacin, dietary fiber, folate, and iron, while ready-to-eat cereals contribute iron, folate, thiamin, vitamin B6, and vitamin B12. Based on the current data presented, encouraging certain grain food patterns in older U.S. adults, including selecting a mix of whole-, enriched-and fortified-grains, from breads, and cereals, may improve nutrient intakes and minimize gaps in shortfall nutrient intakes. In contrast, eliminating grains, especially refined grains, from the diet may lead to unintended nutrient intake consequences. Developing dietary strategies that are mindful of recommended caloric needs, while monitoring nutrients to limit (i.e., added sugars, sodium and saturated fat) can benefit from the inclusion of refined/enriched and whole grain selections in the U.S. diet.
Author Contributions: Y.P. and V.L.F., III collaborated on the intellectual conception and interpretation of the research; V.L.F., III collaborated on the intellectual conception and design of the research and conducted the final analyses; Y.P. drafted the manuscript and both Y.P. and V.L.F., III approved the final manuscript version of the present research.
Funding: The present research was funded and supported by the Grain Foods Foundation in Washington, D.C.

Conflicts of Interest:
The authors declare no conflict of interest. The funding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results. Yanni Papanikolaou, as Vice-President of Nutritional Strategies provides food, nutrition and regulatory affairs consulting services for food and beverage companies and food-related associations and collaborates with Victor L. Fulgoni on NHANES analyses. Victor L. Fulgoni, III, as Senior Vice-President of Nutrition Impact, provides food and nutrition consulting services for food and beverage companies. Victor L. Fulgoni also conducts analyses of NHANES data for members of the food industry.