Current Sodium Intakes in the United States and the Modeled Effects of Glutamate Incorporation into Select Savory Products

Most Americans have dietary sodium intakes that far exceed recommendations. Given the association of high sodium with hypertension, strategies to reduce sodium intakes are an important public health target. Glutamates, such as monosodium glutamate, represent a potential strategy to reduce overall intakes while preserving product palatability; therefore, this project aimed to model sodium replacement with glutamates. The National Cancer Institute method was used to estimate current sodium intakes, and intakes resulting from glutamate substitution (25%–45%) in a limited set of food groups for which substitution is possible. Data sets for individuals aged ≥1 year enrolled in the U.S. National Health and Nutrition Examination Survey 2013–2016 (n = 16,183) were used in the analyses. Glutamate substitution in accordance with the U.S. Department of Agriculture’s food codes was modeled by conservatively altering estimates of sodium intake reductions derived from the published, peer-reviewed literature. The addition of glutamates to certain food categories has the potential to reduce the population’s sodium intake by approximately 3% overall and by 7%–8% among consumers of ≥1 product category in which glutamates were substituted for sodium chloride. Although using glutamates to substitute the amount of sodium among certain food groups may show modest effects on intakes across the population, it is likely to have a more substantial effect on individuals who consume specific products.


Introduction
Dietary sodium reduction is an important goal for the improvement of public health, as reduced sodium intake has been shown to decrease hypertension risk [1]. Hypertension is a valid surrogate endpoint reflective of risks for a myriad of cardiovascular diseases, a leading source of mortality in U.S. adults [2]. Many multifaceted policy and education initiatives aimed at reducing sodium intakes have been ongoing for decades. It has been estimated that a 40% reduction in the U.S. population's intake of sodium over 10 years may save at least 280,000 lives [3] and drastically reduce the number of disability-adjusted life years (DALYs). Despite ongoing public health education and policy initiatives, the preponderance of the U.S. population exceeds current recommendations for sodium intake [4]. Among hypertensive adults, 86% exceed 2300 mg dietary sodium/day [5].
Trends in sodium intakes have not changed over the past 10 years (five U.S. National Health and Nutrition Examination Survey (NHANES) cycles) [6]. Those with the lowest household education, non-Hispanic black race/Hispanic origin, and lowest income have seen the largest increase in sodium adults (≥19 years), excluding those aged ≤19 years (n = 6071), yielding a final analytic sample size of 10,112 U.S. adults (≥19 years).

Demographic Data
All demographic data used for this analysis, including data on sex and age, were collected from participants using the computer-assisted personal interview system during the household interview. Age was categorized to be consistent with the dietary reference intake (DRI) age groups, defined as 1-3, 4-8, 9-13, 14-18, 19-30, 31-50, 51-70, and ≥71 years, and was used to compare estimates of sodium intakes. Children and adults were defined as those individuals who were aged 1-18 and ≥19 years, respectively.

Dietary Sodium Intake
NHANES participants were asked to complete two 24-hour dietary recalls for the collection of dietary intake data. The first 24-hour dietary recall was self-reported in the MEC and collected in person by trained NHANES interviewers. The second 24-hour dietary recall interview was completed via telephone approximately 3-10 days after the MEC examination. Both 24-hour recalls were collected by trained interviewers using the U.S. Department of Agriculture's (USDA) validated, automated, multiple-pass method [23,24]. Proxy respondents provided dietary intake data for young children and proxy-assisted interviews were utilized for children aged 6-11 years. Questionnaires, data sets, and all related documentation from each NHANES cycle can be found on the NCHS website [25]. The USDA Food and Nutrient Database for Dietary Studies was used to convert foods and beverages (as reported) to their respective sodium intake values [26].

Comparison to DRI Values
The DRIs are a set of nutrition reference values, defined by the National Academies of Sciences, Engineering and Medicine (NASEM) Food and Nutrition Board, that are designed to assess nutrient intakes of healthy people and establish guidelines for risk assessment in the United States and Canada [27]. The DRIs for sodium and potassium were recently updated in 2019, and for the first time, a new category of DRIs based on chronic disease, called the chronic disease risk reduction (CDRR), was established for sodium [1]. Other DRIs established by the NASEM for sodium include the estimated average requirement, recommended dietary allowance, adequate intake, and tolerable upper intake level (UL). DRI values differ for individuals based on age and sex [1]. Sodium was reported as usual intake and the proportion of the population with intakes above the CDRR and UL. Information regarding the recent DRIs for sodium and potassium can be found in the NASEM report, Dietary Reference Intakes for Sodium and Potassium [1].

Sodium Intake Modeling
Glutamates, such as MSG, are flavor enhancers that have been effectively used to reduce sodium in certain food categories, particularly in savory products. A review of the scientific literature demonstrates that glutamates have been utilized to reduce sodium among various mainstream products (Table 1). Assuming that the food supply already contains a significant amount of glutamates and that amounts used among products vary, we made conservative assumptions, in consultation with food scientists, of a 25%-45% reduction in sodium by substitution of sodium chloride with glutamate salts across certain categories of foods using the USDA food codes ( Table 2). Consumers of glutamates were those who reported consumption of one or more food categories in which glutamates were substituted for sodium chloride. Table 1. Sodium reduction in various food products with the incorporation of glutamates.

Statistical Analyses
The National Cancer Institute (NCI) method was used to determine estimates of usual intake of sodium from the diet. Covariates used in the NCI model were as follows: (1) sequence of 24-hour recall (first or second dietary recall); and (2) day of the week the 24-hour recall was collected (weekend/weekday). All statistical analyses were performed using SAS software (version 9.3; SAS Institute Inc., Cary, NC, USA). SAS macros necessary to fit this model and to perform estimation of usual intake distributions, as well as additional details and resources concerning the NCI Method, are available via the NCI website [30]. The fitted model is a two-part model that first uses logistic regression to estimate the probability of intake consumption for each consumer, and then, secondly, uses linear regression to estimate the actual daily amount of intake on a transformed scale, while taking into account within-person variation [30]. Sample weights were used to account for differential nonresponse and noncoverage and to adjust for planned oversampling of some groups, in order to generate a nationally representative sample. Standard errors for all statistics of interest were approximated using Fay's modified, balanced, repeated-replication technique [31,32].

Results
3.1. Current Mean Sodium Intakes, Percentages above the CDRR, and Percentages above the UL Overall, sodium intakes among the general U.S. population are higher than federal recommendations. On the basis of NHANES 2013-2016 data, Americans (aged >1 year) consume approximately 3361 mg sodium/day on average (Table 3). Mean daily sodium intake from foods and beverages among the U.S. population was 2906 mg/day for children (aged 1-18 years) and 3499 mg/day for adults (aged ≥19 years). Table 3. Estimated and potential means usual sodium intake (in milligrams) from dietary sources and the estimated percentages of mean usual-sodium intakes greater than the CDRR and UL in the U.S. population (aged ≥1 year) by age and sex, NHANES 2013-2016 1,2

Age (Years)
n Current Intake Potential Intake  Regardless of age, men had higher sodium intakes than women. Specifically, among adults (≥19 years), men typically consumed approximately 4067 mg sodium/day, whereas women only consumed approximately 2956 mg sodium/day. Similar themes were apparent among children (1-18 years); boys had higher mean sodium intakes than girls (3268 versus 2673 mg/day, respectively). Therefore, women of all ages were less likely to exceed the CDRR and UL compared to men.
Across age subgroups, sodium intake was highest among men and women aged 19-30 years (4431 versus 3138 mg/day, respectively) and varied across the life course. For men, sodium intake increased with age in the adolescent years (1-18 years), plateaued among early adulthood (19-30 years), and then decreased through the remainder of adulthood (≥31 years). However, slightly different patterns were observed among women. Whereas sodium intakes among young girls increased with age until 9-13 years, a slight decrease in intake was observed between the ages of 14-18 years, followed by an increase in intake from 19-30 years, and lastly, a final decrease in intake for the remainder of adulthood (≥31 years). Older adults (≥71 years) had the lowest sodium intakes of all adult participants among both men and women. Thus, younger adults were more likely to exceed the CDRR and UL for sodium compared to their older adult (≥71 years) counterparts. Among children, boys and girls in the 4-8-year and 9-13-year life stages had the highest prevalence of exceeding the CDRR and UL.
Estimated mean sodium intake and the percent-wise contributions for selected food categories to total sodium intake in the diets of U.S adults (≥19 years) and children (1-18 years) are presented in Tables 4 and 5. On a population level, no individual food group contributes large amounts of sodium to the diet; sodium intakes appear to be widespread throughout the food supply. However, the savory food groups represented in Tables 4 and 5 provide much larger proportions of sodium to the diets of those who consumed these products (i.e., "consumers"). For example, meat-based frozen meals provide 0.3% of the sodium present in the diets of all U.S adults, but as much as one-third (32%) among consumers. Among children, the top three contributors to total sodium intakes are crackers and salty snacks, cured meats, and select cheeses (Table 5). Although intakes of these select food categories remain high overall, intakes among consumers of these categories are significantly higher than the general population of U.S. children (Figure 1). For cured meats in particular, children who consume these products receive 20% of their usual sodium intake from this source, whereas cured meats account for only 4% of total sodium intakes among the general population of U.S. children. Table 4. Estimated mean sodium intake (in milligrams) and percentage-wise contributions from selected food groups in the diets of U.S. adults (aged ≥19 years) by age and sex, NHANES 2013-2016 1,2,3 .

Figure
All Adults Men Women  3 Unlike the National Cancer Institute-adjusted statistics that represent long-term, usual dietary intake estimates presented in Table 3, the food intake statistics here are estimates of intake on any given day. The above sample sizes for consumers reflect a categorization of the NHANES respondents based on whether they reported sodium intakes in one of the above categories, and describe the sample, not the population. Estimates reflective of population intakes for the above categories are indicated by "all adults," "all men," and "all women," respectively. * Estimates have SEs of concern or sample sizes of concern.   2 The analytic sample includes individuals aged 1-18 years who were not pregnant or lactating and had complete information for age and 24-hour dietary recall on day one. 3 Unlike the National Cancer Institute-adjusted statistics that represent long-term, usual dietary intake estimates presented in Table 3, the food intake statistics here are estimates of intake on any given day. The above sample sizes for consumers reflect a categorization of the NHANES respondents based on whether they reported sodium intakes in one of the above categories, and describe the sample, not the population. Estimates reflective of population intakes for the above categories are indicated by "all adults," "all men," and "all women," respectively. * Estimates have SEs of concern or sample sizes of concern. Nutrients 2019, 11, x FOR PEER REVIEW 9 of 15

Models of the Effects of Gutamates on Mean Usual Sodium Intakes, Percentages Above the CDRR, and Percentages Above the UL
Universal incorporation of glutamates into the select savory food groups (presented in Table 2) would result in a 3% (162 mg/day) reduction in overall sodium intakes in the U.S. population (aged ≥ 1 year) and a 7-8 percentage point reduction among consumers of one or more food categories in which sodium chloride could be substituted for by glutamates. Among U.S. children specifically,  Table 2) would result in a 3% (162 mg/day) reduction in overall sodium intakes in the U.S. population (aged ≥ 1 year) and a 7-8 percentage point reduction among consumers of one or more food categories in which sodium chloride could be substituted for by glutamates. Among U.S. children specifically, glutamates have the potential to reduce the proportion of the population exceeding the UL for sodium by 5 percentage points (Table 3) and to reduce consumer intakes by 211-263 mg/day among boys and girls. Likewise, glutamates could reduce the sodium intakes of consumers by 321 and 236 mg/day in adult men and women, respectively (Tables 6 and 7).  1 MSG, monosodium glutamate; NHANES, National Health and Nutrition Examination Survey; SE, standard error. 2 The analytic sample included individuals aged ≥ 19 years who were not pregnant or lactating and had complete information for age and 24-hour dietary recall on day one. 3 Unlike the National Cancer Institute-adjusted statistics that represent long-term, usual dietary intake estimates presented in Table 3, the food intake statistics here are estimates of intake on any given day. The above sample sizes reflect a categorization of the NHANES respondents based on whether they reported sodium intakes in one of the above categories, and describe the sample, not the population. * Estimates have SEs of concern or sample sizes of concern.   2 The analytic sample includes individuals 1-18 years old who were not pregnant or lactating and had complete information for age and 24-hour dietary recall on day one. 3 Unlike the National Cancer Institute-adjusted statistics that represent long-term, usual dietary intake estimates presented in Table 3, the food intake statistics here are estimates of intake on any given day. The above sample sizes reflect a categorization of the NHANES respondents based on whether they reported sodium intakes in one of the above categories, and describe the sample, not the population. * Estimates have SEs of concern or sample sizes of concern.

Discussion
Dietary factors are among the top contributors to chronic disease risk and DALYs in the United States. High intake of sodium is one risk factor that has been identified as a contributor to this burden [33]. According to our analysis, current estimates of mean usual sodium intake remain high across all age and sex subgroups of the U.S. population, and they continue to exceed authoritative recommendations, consistent with previous reports [4,6]. Contrary to prior reports [6], age-related differences in estimated usual intakes did not appear to be more pronounced in men than women (Table 3). Our analyses provide unique data on the diets of consumers of select food categories. Although reducing the amount of sodium among certain food groups may show modest effects on intakes across the population, it may have a large effect on individuals who consume these types of products. For example, about 18.7% of U.S. adults consume cured meats on any given day; reducing sodium intake of cured meat products by 40% would have a large impact on those consumers, since cured meats account for 21% of their total sodium intake from the diet. Figure 1 illustrates substantial effects of incorporating glutamates into crackers and salty snacks, cured meats, and select cheeses on U.S. children (1-18 years). Given current sources of sodium in the diets of young children, glutamate's use in these select categories may have the greatest impact on sodium intakes in this age group. Meat-based frozen meals, vegetable and meat-based soups, and cured meats contain the highest amounts of sodium; however, grain products were previously shown to be the largest contributor of sodium intakes to the U.S. diet because they are more ubiquitously consumed [6]. Consumer sentiment around MSG has deterred many consumer-packaged food companies from utilizing it to reduce sodium intake in products [34].
Several other strategies have been applied to reduce the population's sodium intake. Gradual reduction through a cumulative series of small decreases over 6 weeks was shown to be effective in reducing the sodium content of white bread by about 25% without altering palatability. However, reduction would need to be applied to all breads on the market to go unnoticed by consumers [35]. Potassium chloride (KCl), calcium chloride (CaCl 2 ), and magnesium sulfate (MgSO 4 ) have been used as substitutes for table salt; however, their bitter taste has limited their use and uptake by consumers [36]. Citric acid in tomato soup [37] and lactic acid in bread [38] have the potential to enhance saltiness and be useful in reducing sodium intake. SODA-LO, a new but more costly sodium-reduction ingredient that can reduce sodium in certain applications through its technology that turns standard salt crystals into free-flowing, hollow salt microspheres, has been shown to deliver taste and function by maximizing surface area in products such as potato chips and baked goods [6].
Current intake above public health recommendations is not solely a United States-centric issue, but a global pandemic demonstrated by high intakes of sodium in other countries [39]. Assuming the accuracy of NHANES and other international databases, ongoing public health education initiatives show no signs of success in decreasing intakes. Frequent use of nutrition labels appears to be associated with lower consumption of sodium and high-sodium foods; however, while surveys suggest that consumers may wish to reduce their sodium intake, it is likely not a priority in what most consumers choose to eat [40]. In fact, evidence indicates that many consumers avoid products labeled as "low sodium" [40]. Reducing intakes through food science and technological advances seems appropriate, in order to make the most impactful reductions in the consumption of sodium at the population level.
Our study has some strengths and limitations to consider. First, the strengths of our analysis are that the models applied to examine usual intakes adjusted for the effects of within-person variation measurement error, and that NHANES is a large nationally representative sample that allows for the estimation of usual intakes of sodium at the population level. However, the limitations of our study should also be noted. This modeling study used conservative assumptions of sodium reduction by substituting glutamates for sodium chloride in several What We Eat in America food categories. We chose these conservative reduction values, presented in Table 2, upon consultation with food scientists, with the hopes of accounting for what is already contained in the food supply so as not to overestimate the total effect of glutamates. Restaurant foods supply a large portion of sodium to the U.S. diet [40]; however, we chose to not model inclusion of glutamates into restaurant foods, since many of these flavor enhancers are already in widespread use in restaurants. Therefore, the effect of glutamates could be greater than what is presented in our study. NHANES also has several limitations, including the reliance on self-reported dietary intake data and assumptions of USDA reference database accuracy for estimating sodium intakes across the population. Self-reported dietary data are prone to systematic errors, such as energy underreporting. Additionally, we cannot completely rule out the potential for self-selection bias; that is, people who participate in nutrition-and health-related research tend to differ by sociodemographic factors and may have been more interested in participating in NHANES [41]. Finally, in order to fully maximize the effectiveness of sodium reduction, the acceptability of MSG among consumers must be taken into consideration [42,43].

Conclusions
Current sodium intakes in the United States remain high and unchanged from previous NHANES cycles, exceeding public health recommendations. The addition of glutamates to certain savory food categories has the potential to help reduce the population's intake of sodium by approximately 3.0%, and to reduce the intake by 7.3% among consumers of the product categories in which sodium chloride could be substituted for by glutamates. While reducing the amount of sodium among certain food groups may show modest effects on intakes across the adult population, it may have a large effect on those who consume those types of products.
Funding: Funding for this manuscript was provided through an unrestricted educational grant from Ajinomoto to Think Healthy Group. The funding body had no role in the design, analysis, interpretation, or presentation of the data and results. The authors and sponsor strictly adhered to the American Society for Nutrition's guiding principles for private funding of food science and nutrition research.