Association of Yogurt Consumption with Nutrient Intakes, Nutrient Adequacy, and Diet Quality in American Children and Adults

The popularity of yogurt has increased among consumers due to its perceived health benefits. This study examined the cross-sectional association between yogurt consumption and nutrient intake/adequacy, dietary quality, and body weight in children and adults. National Health and Nutrition Examination Survey 2001–2016 data (n = 65,799) were used and yogurt consumers were defined as those having any amount of yogurt during in-person 24-h diet recall. Usual intakes of nutrients were determined using the National Cancer Institute method and diet quality was calculated using the Healthy Eating Index-2015 (HEI-2015) scores after adjusting data for demographic and lifestyle factors. The data show that approximately 6.4% children and 5.5% adults consume yogurt, with a mean intake of yogurt of 150 ± 3 and 182 ± 3 g/d, respectively. Yogurt consumers had higher diet quality (10.3% and 15.2% higher HEI-2015 scores for children and adults, respectively); higher intakes of fiber, calcium, magnesium, potassium, and vitamin D; and higher percent of the population meeting recommended intakes for calcium, magnesium, and potassium than non-consumers. Consumption of yogurt was also associated with lower body weight, body mass index (BMI), and 23% showed a lower risk of being overweight/obese among adults only. In conclusion, yogurt consumption was associated with higher nutrient intake, nutrient adequacy, and diet quality in both children and adults.


Introduction
Fermented foods have played an important role in human health for centuries because of their enhanced preservation and functional properties [1]. The popularity of fermented foods has steadily increased among consumers because of their link to improved health. Yogurt is a semisolid fermented milk product produced by lactic acid-producing bacteria Lactobacillus bulgaricus and Streptococcus thermophilus [2]. Similar to other fermented foods, yogurt production has increased by over 4% between 1995 and 2019 [3] and, correspondingly, yogurt intake has steadily increased in the past decade [4]. Yogurt has higher amounts of protein, vitamin B 2 , vitamin B 12 , calcium, magnesium, potassium, and zinc than milk [5]. Yogurt may provide additional health benefits beyond nutrient provision because it contains unique bioactive compounds and live and active cultures [6].
An accumulating body of scientific evidence suggests that yogurt and fermented dairy consumption may be associated with improved cardiometabolic health [7][8][9]. Meta-analyses have shown that yogurt intake is linked with lower risk of type 2 diabetes [10,11], cardiovascular disease [12], metabolic syndrome [13], and with lower risk of cardiovascular-and all-cause mortality [14]. Higher yogurt

Statistical Analysis
All analyses were performed using SAS 9.4 (SAS Institute, Cary, NC, USA) software. The data were adjusted for the complex sampling design of NHANES, using appropriate survey weights, strata, and primary sampling units. Day one dietary/examination weights were used in all intake analysis and Mobile Examination Center weights were used for anthropometric variables.
Least square means (LSM) and standard errors (SE) were generated for energy and nutrient intake, food group intake, diet quality, and anthropometric variables in yogurt consumers and non-consumers via regression analyses. Analyses were adjusted for age, gender, ethnicity, poverty income ratio, physical activity level, current smoking status, and alcohol (only for those 19 years and older), and kcal (except for energy and HEI-2015). Usual intakes of nutrients were determined using the National Cancer Institute (NCI) method [36] and the NCI macros (Mixtran and Distrib) were used to generate parameter effects after covariate adjustments and to estimate the distribution of usual intake (UI). The one-part NCI model was used for nutrients since these substances are consumed on most days by most subjects. Covariates for usual intake estimation included day of the week of the 24-h recall [coded as weekend (Friday-Sunday) or weekday (Monday-Thursday)] and sequence of dietary recall (first or second), and variance estimates were obtained using the two days of intake with one-day sampling weights. The percentage of the population below the Estimated Average Requirement (EAR) or above Adequate Intake (AI) of nutrients was assessed using the cut-point method (except for iron where the probability method was used) and Z-statistic was used to assess differences between non-consumers and yogurt consumers. Logistic regression was utilized to assess the association of yogurt consumption with risk of overweight/obesity in children and adults. p < 0.01 was considered statistically significant.

Yogurt Intake
Approximately 6.4% of children and 5.5% of adults consume yogurt. Yogurt consumers were 3.0 and 2.6 years younger than non-consumers in children and adults, respectively. While in children a similar percentage of males/females consume yogurt, a smaller percentage of adult males consume yogurt. A greater percentage of yogurt consumers were non-Hispanic White (and a lower percentage yogurt consumer were non-Hispanic Blacks) as compared to non-consumers in both children and adults. A greater percentage of yogurt consumers had a household income >1.85 the poverty level and a lower percentage yogurt consumer had a household income <1.35 the poverty level as compared to non-consumers in both children and adults (Supplementary Table S1). The mean intake of yogurt (on day 1 of recall) among consumers was 150 ± 3 g/d (95th percentile 307 g/d) and 182 ± 3 g/d (95th percentile 337 g/d) among children and adults, respectively. Median intake was 122 g/d in children and 169 g/d in adults. Mean per capita intake of yogurt (on day 1 of recall) was 11.6 ± 0.5 and 12.9 ± 0.5 g/day among children and adults, respectively, and has significantly increased (β = 0.59 g/cycle, p = 0.0164 for children; β = 1.46, g/cycle p < 0.0001 for adults) over the last eight NHANES cycles (2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)

Link Between Yogurt Intake and Diet Quality
Intake of yogurt was associated with 10.3% and 15.1% higher HEI-2015 scores (p < 0.01) in children and adults, respectively ( Table 4). The HEI-2015 subcomponent scores for 'greens and beans,' 'total fruit,' 'whole fruit,' 'whole grain,' 'dairy,' 'seafood and plant protein,' 'sodium,' 'refined grains,' and 'saturated fat' were higher (p < 0.01) in consumers compared to non-consumers for both children and adults. Additionally, adult yogurt consumers had a higher score for 'added sugar' and a lower score for 'fatty acids ratios' (p < 0.01 for all).
Intake of yogurt was also linked with significant differences (p < 0.01) in specific MyPlate food groups [33]. Yogurt consumers compared to non-consumers had higher intakes of total dairy (+21.9% in children; +38.7% in adults), total fruit (+26.7% in children; +49.5% in adults), whole fruit (+36.7% in children; +66.7% in adults), and whole grain (+25.4% in children; +44.3% in adults) (Figure 1). Values are least square means ± standard error of means, adjusted for age, gender, ethnicity, poverty income ratio, physical activity level, current smoking status, and alcohol (only for ≥19 years), and kcal. p values are for difference between consumers and non-consumers.

Discussion
This is the first report to investigate the association between yogurt consumption and nutrient intakes, nutrient adequacy, diet quality, and weight status in a nationally representative population of American children and adults. Combining data from eight cycles of NHANES, the present analysis showed that yogurt consumption was associated with higher nutrient intakes and better nutrient Nutrients 2020, 12, 3435 9 of 14 adequacy, as well as a higher diet quality score compared with non-consumers for both children and adults. Furthermore, weight-related outcomes were better in adult yogurt consumers when compared to non-consumers.
Approximately 6% of Americans consumed yogurt on day 1 of the NHANES 24-h dietary recall. The prevalence of yogurt consumption in American children and adults in the present analysis is less than recent estimates in British and Canadian population groups [21,22]. Using data from the National Diet and Nutrition Survey, Hobbs et al. [21] reported that about 62% of children aged 4-10 years and 31% of children aged 11-18 years were yogurt consumers. Similarly, Vatanparast et al. [22] analyzed data from Canadian Community Health Survey 2015 and found 20% Canadians consumed yogurt on a given day. The prevalence of yogurt consumption observed in this study is close to those by Keast et al. [25], who estimated that 8.5% of children and adolescents age 8-11 years were yogurt based on data from NHANES 2005-2008. Other estimates indicated that 33% children age 2-18 years (NHANES 2003(NHANES -2006, and 41% men and 64% women (Framingham Heart Study Cohorts 1998-2001, 2002-2005 consumed yogurt at least once per week [23,24]. While the prevalence observed in our analysis appears low, on a population basis this represents about 12 million individuals. The mean intake of yogurt in this study are higher than the 135 g/d intake estimate for the Canadian population [22] and a 108 g/d intake tertile II estimate for 8-11-year-old British children [21]. In this analysis, the mean intake of yogurt among consumers was 5.3 fluid oz/d (0.66 cups or 162 g) for children and 6.4 fluid oz/d (0.8 cups or 196 g) for adults, which represents approximately 0.9 servings per day for children and 1.1 servings per day for adults. Thus, regular yogurt consumption may significantly contribute to meeting the DGA recommendations for dairy foods.
Yogurt consumers had significantly higher intakes of fiber, calcium, magnesium, potassium, vitamin A, vitamin B 6 , vitamin B 12 , vitamin C, and vitamin D than non-consumers. Along those lines, yogurt consumers also had a higher nutrient adequacy for fiber, calcium, magnesium, potassium, vitamin A, and vitamin B 12 than non-consumers. Many of these nutrients are currently under-consumed by Americans and have been identified as "shortfall nutrients" by the DGA [30]. Additionally, the DGA has classified dietary fiber, calcium, potassium, and vitamin D as "nutrients of public health concern" because their current intakes are low enough to impact one's health [30]. Similar observations were also reported in earlier cross-sectional studies from both US and international cohorts [21][22][23][24][25]. Since yogurt is a good source of several of the above nutrients [37-41], yogurt consumption is naturally expected to lead to more nutrient dense diets and greater adequacy for nutrients. Finally, children and adult consumers of yogurt compared to non-consumers had 176 and 223 mg/d lower intakes of sodium respectively. High sodium intake has been linked to elevated blood pressure and therefore reducing dietary sodium is an important target for public health improvement [30].
As yogurt is not a good source of fiber and vitamin C, the results suggest that yogurt consumers are eating higher amounts of other healthy foods as well. Indeed, this was reflected in the fact that both children and adult yogurt consumers had better diet quality scores than non-consumers. Diet quality was assessed by HEI-2015 [31] in the present analysis. HEI is a validated measure of diet quality and is indicative of compliance/adherence of a person's diet to the eating pattern recommended by the DGA [30]. HEI is commonly used to evaluate diets in population groups [42], food environments [43], to assess changes in the diet quality over time [44], and to validate other nutrition research tools and indexes [45]. It has also been used in recent research to understand relationships between nutrients/foods/dietary patterns and health-related outcomes [46][47][48][49]. In the present analysis, HEI-2015 total scores of yogurt consumers were significantly higher for children and adults than their respective non-consumers, indicating a higher compliance to nutritional guidelines. These results are consistent with earlier cross-sectional analyses, which found that yogurt consumers have a significantly higher diet quality than non-consumers [21][22][23][24][25]. HEI-2015 has 13 subcomponents (nine for adequacy and four for moderation) [31] and the scores for 9 and 10 subcomponents were also significantly higher for children and adult consumers. It is interesting to note that not only were the HEI-2015 subcomponent scores related to dairy, fruits, vegetables, and whole grain higher, the actual intakes of these food groups were also significantly higher in yogurt consumers than non-consumers. This is important because current intakes of these food groups are lower than the recommended amounts in the USDA's Healthy US-Style Eating Pattern [30]. Indeed, the majority of the US population currently does not meet the daily intake recommendations for fruits (nearly 80%), vegetables (nearly 90%), whole grain (nearly 100%), and dairy (nearly 80%) [37].
In the current study, adult yogurt consumers had a lower weight, BMI, and waist circumference than non-consumers and yogurt consumption was significantly associated with lower odds of being overweight or obese and having an elevated waist circumference. This is an interesting finding since adult yogurt consumers also had about a 5% higher calorie intake. One potential explanation for this observation is the presence of live and active cultures in yogurt. Yogurt contains the starter cultures S. thermophilus and the L. delbrueckii subspecies bulgaricus which are thought to contribute to heath. Other Bifidobacterium and Lactobacillus strains are sometimes added as probiotics, which are live microorganisms that when consumed in adequate amounts confer a health benefit in the host [50]. It has been hypothesized that the either the starter cultures, the probiotics, or the combination can beneficially impact the gut microbiota composition and function [6,51]. Thus, the observed link between yogurt consumption and better body composition could be driven by changes in the microbiota that are impacting energy metabolism. Since the present analysis did not distinguish between those yogurts that contain just the starter cultures and those with added probiotics, nor did it compare yogurts with live cultures to pasteurized products, additional work is needed to further elucidate the role of fermentation-associated microbes on weight and body composition. A healthier dietary pattern (higher intakes of fruits and vegetables, whole grain, and dairy) as observed in our analysis for yogurt consumers, along with potentially other lifestyle differences (e.g., more physical activity among yogurt consumers), could help explain the current findings of a lower body weight, BMI, and waist circumference and lowered risk for obesity. The results of this study are congruent with those from other cross-section studies that have shown that yogurt consumption was associated with a lower BMI, lower body weight/weight gain, and smaller waist circumference [21,22,25]. This finding may have important health and economic implications as more than one third of US adults are obese [52], and obesity is associated with several health risks [53] with annual medical costs amounting to $147 billion [54].
The regular consumption of added sugars from certain products has been associated with an increased risk of obesity [55][56][57]. The DGA recommends limiting intake of added sugars to less than 10% of total daily calories as part of a healthy diet [30]. More recently, the 2020 Dietary Guidelines Advisory Committee recommended that the intake of added sugars be lowered to 6% of total calories given their impact on health [58]. Flavored yogurts have the same nutrition profile as plain yogurts. The data presented herein showed that the intake of added sugars was nearly identical between non-consumers and consumers in both children and adults (Table 2), indicating that yogurt consumption was not linked to higher intakes of added sugars in this cohort. This study examined the short-term impact of yogurt intake on nutrient adequacy and body composition and did not distinguish between flavored and plain yogurts. Thus, additional work is needed to more fully understand the link between long term flavored yogurt intake and health.
The strengths of this study include the use of a large nationally representative sample achieved through combining several sets of NHANES data releases and the use of numerous covariates to adjust data to remove potential confounding. A major limitation of this study is the use of a cross-sectional study design, which cannot be used to determine cause and effect. The dietary intake data were self-reported recalls relying on memory and are potentially subject to reporting bias. Finally, while we accounted for a number of covariates in our statistical models, residual confounding cannot be ruled out.

Conclusions
In conclusion, the results showed that yogurt consumption was associated with higher nutrient intake, better nutrient adequacy, and better diet quality in both children and adults. Additionally, yogurt consumption was linked to a lower body weight and related parameters in adults. Long-term randomized controlled trials are needed to further examine the effects of yogurt consumption on body weight. Encouraging yogurt consumption may be an effective strategy for improving intakes and adequacy of certain nutrients and achieving a healthier dietary pattern.

Author Contributions:
The authors' responsibilities were as follows: C.J.C.: Project conception, designed research, developed overall research plan, and participated in revising the manuscript; S.A.: Participated in interpretation of the data, prepared the first draft of the manuscript, and participated in revising the manuscript; V.L.F.III: Designed research, developed overall research plan, analyzed data, performed statistical analysis, and participated in interpretation of the data and revising the manuscript; All authors have read and agreed to the published version of the manuscript.

Funding:
The study and the writing of the manuscript were funded by the National Dairy Council, Rosemont, IL, USA.