Correspondence: JA DeSimone, Department of Physiology and Biophysics, Virginia Commonwealth University, Richmond, Virginia, USA. VCU School of Medicine, 1101 East Marshall Street, P.O. Box 980551, Richmond, Virginia 23298-0551, USA. E-mail: email@example.com, Phone: +1-804-828-9756. Please copy: C Gaine, ILSI NA, 1156 Fifteenth St NW, Suite 200, Washington, DC 20005, USA. E-mail: firstname.lastname@example.org, Phone: +1-202-659-0074, Ext. 121, Fax: +1-202-659-3859.
This article is based on proceedings from the Symposium on Sodium in the Food Supply: Challenges and Opportunities, sponsored by the North American Branch of the International Life Sciences Institute, at Experimental Biology 2010 in Anaheim, California. The symposium aimed to address the issue of dietary sodium and its consequences for public health. Presenters spoke on a variety of key topics, including salt taste reception mechanisms and preferences, methods and measures to assess sodium in the US food supply, and considerations regarding the reduction of sodium in processed foods. Information from these presentations, as well as literature references, are provided in this article.
There is growing concern regarding dietary sodium and its consequences for public health. To address this issue, the North American branch of the International Life Sciences Institute assembled the Symposium on Sodium in the Food Supply: Challenges and Opportunities, which was held at Experimental Biology 2010 in Anaheim, California. At the time of the symposium, the Institute of Medicine (IOM) had recently recommended that the US daily sodium intake levels be significantly lowered. The IOM reported that actual sodium intake was at least 50% higher than the level recommended in the Dietary Guidelines for Americans (DGA), which then was 2,300 mg/day. The 2010 Dietary Guidelines Advisory Committee subsequently recommended that the sodium content of foods in the marketplace be immediately and deliberately reduced to allow consumers to decrease daily sodium intake to <2,300 mg, aiming at an ultimate target intake of 1,500 mg.
There is consensus that increased sodium intake can cause increased blood pressure, which in turn can increase the risk for cardiovascular and renal disease, but controversy exists regarding the size of the effect, which subpopulations are at greatest risk, and how the potential health benefits of a reduction in sodium intake are likely to be distributed across the population. Although these issues remain open topics of discussion, the IOM report concludes the preponderance of evidence to date justifies the view that excess sodium intake is a significant public health risk for the entire population and, accordingly, that the sodium content of foods should be regulated by the US Food and Drug Administration (FDA). It was recommended that mandated reductions in the sodium content of foods be carried out in a gradual stepwise manner to allow the population to adapt to the lower sodium content of processed and restaurant foods without affecting palatability, and to assess issues such as undesired and unacceptable changes in food physical properties and food safety. There are also issues related to potential adverse physiological responses to sodium reduction such as elevated blood pressure (reverse salt sensitivity) and a rise of plasma renin activity with consequent cardiovascular events.
Ensuring palatability, safety, and desirable physical properties of food may be formidable challenges for the food industry as attempts are made to lower food sodium content. Moreover, one largely unexplored question is the feasibility of formulating balanced diets that meet the DGA and that also maintain sound nutrition, given the constraints of the sodium content of the current food supply and that of projected reduced-sodium supplies. These and additional challenges were identified, analyzed, and discussed at the Experimental Biology 2010 symposium by the speakers, including Drs. Victor Fulgoni, Gary K. Beauchamp, Adam Drewnowski, and Guy H. Johnson, as well as by the audience. The outcomes stated in this paper were drafted by the speakers, and each section is the sole responsibility of its respective author: salt taste (Beauchamp); assessing sodium in the US food supply (Drewnowski), and considerations regarding the reduction of sodium in processed foods (Johnson).
Sodium chloride, herein referred to as “salt,” is the most common mineral that humans consume. Sodium is required for life and the body does not efficiently store it, hence the need to consume it regularly. In healthy individuals, there is a remarkably efficient system to excrete sodium when it is consumed in excess and to retain it when dietary sources are limited.[5, 6] A growing body of evidence (reviewed in Henney et al.) has linked excess salt intake to compromised cardiovascular function. In addition, a vast number of health organizations throughout the world have recommended substantial reductions in salt intake on a population-wide basis. To accomplish this goal, it is necessary to understand the factors that drive high salt consumption before successful strategies to reduce it can be rationally designed. The most significant of these factors is the role of taste in modulating intake. This section briefly describes the mechanisms underlying salt taste perception. The varied roles of salt in foods, as well as the factors influencing human salt preferences, are also discussed. Finally, research needs are briefly outlined. More in-depth reviews on this topic can be found in Henney et al. and Beauchamp and Stein.
Mechanisms of salt taste perception
During the past decade, remarkable progress has been made in understanding the molecular mechanisms underlying detection and perception of sweet, bitter, and umami tastes (see Bachmanov and Beauchamp for a review). However, the identification of salt taste mechanisms has been much slower. In 2010, two research groups[9, 10] independently definitively demonstrated that one long-suspected receptor,[11-13] the epithelium sodium channel, ENaC, is involved in sodium recognition in taste cells. Thus, common mechanisms underlie salt taste perception and sodium regulation in other tissues such as the kidney, where ENaCs play a prominent role.
The ENaC is not the sole explanation for salty taste perception, however. At least one other, currently unknown, molecular receptor underlies salt taste. The importance of this non-ENaC mechanism is demonstrated by the fact that animal models that have either genetically or pharmacologically disabled ENaC exhibit vigorous residual neural and behavioral responses to salt. One possibility is that the ENaC is responsible for the quality of “saltiness,” whereas an unknown receptor is responsible for other sensory attributes of salt, such as its ability to convey body or thickness to an ingested food. Inconsistent with this hypothesis is the clear salty taste imparted by potassium chloride, which some consumers also perceive as tasting bitter, metallic, or “dirty.” ENaCs do not respond robustly to potassium chloride; therefore, it would seem that some other receptor must also be involved in saltiness perception. Clearly, additional research is needed to completely explain salt taste reception, which is an important goal if one wants to develop novel salty taste replacers or enhancers (see below).
Sensory roles of salt in foods
The most obvious sensory role of salt is to make food taste pleasantly salty. However, salt is a multifunctional ingredient that can also act as a preservative, insure various favorable functional characteristics of prepared foods, and enhance food flavor and lend “body.” Another function of salt is to suppress the off flavors of foods, which is accomplished, in part, through the remarkable ability of sodium to inhibit the bitterness of many food compounds. By inhibiting bitterness in a complex food, salt can enhance more positive flavor attributes such as sweetness, which is at least one way that salting foods can enhance flavor without necessarily adding substantial perceived saltiness. Actions designed to reduce the amount of salt in foods must therefore contend not only with how lowering the perceived saltiness of a food impacts hedonic quality, but also with how reductions of added salt impact these other flavor attributes. In addition, any practical replacement or enhancement strategy must also be cognizant of these non-salty sensory functions.
Human salt preference: origin and development
The vast literature on salt taste perception in sodium-depleted animals has revealed exquisite regulatory mechanisms that can insure intake.[5, 6, 16] However, because humans are very rarely actually depleted of salt (virtually everyone consumes 1 or 2 orders of magnitude more than the physiological minimum needed for life), these regulatory mechanisms cannot explain humans’ desire for salt and salty foods even though they have no “need” for sodium. Two mechanisms have been postulated to explain this desire: an innate liking for salt and conditioning or imprinting on salt taste. Similarly to most cases in which this dichotomy is proposed, it is most likely that there is a complex combination of both mechanisms.
An examination of the origins of human salt taste preference, both historically and developmentally, may shed light on the factors underlying human liking for salt when it is not needed. Historically, it is often said that salt was first added to food 10,000 or more years ago to act as a preservative and humans consequently became familiar with eating salty foods, which somehow resulted in them developing a desire for salty tastes. The difficulty with this explanation is that there is no real evidence that the cause-and-effect arrow went in this direction. It is just as likely that humans discovered they liked salt and that this led them to discover its preservative functions. In any case, this explanation requires that something about consumption leads to enhanced liking. Indeed, in his influential book Neptune's Gift: A History of Common Salt, Multhauf calls salt the original narcotic, implying a pharmacological reinforcing effect (presumably innate) independent of need.
Current high salt intakes have been attributed to the widespread use of salt in manufactured foods. However, there are reasons to believe that such intakes may be a consequence of human liking rather than a driving force. First, the evidence that humans have increased salt intake as the consumption of manufactured foods has increased is not convincing. This observation is partly due to the paucity of solid information on salt intake prior to the second half of the 20th century. Second, as demonstrated most clearly by data from the Intersalt study, salt intake is relatively and consistently high across many cultures, some of which do not consume mainly manufactured foods. Indeed, it has been estimated that in one part of China in 300 bc, intakes were comparable with those consumed in the developed world today. These data have been used to argue that physiological factors underlie the supposed excess intake of salt by humans, but the evidence supporting this interesting hypothesis is not strong and one small study directly testing whether humans regulate salt intake did not show significant results.
One question is whether studies of human development of salt intake can help clarify the basis for our desire for salt. Unlike the case for sweetness, salt preferences have not been observed in newborn human infants. Beginning at about 4 months of age, infants exhibit a preference for salty water relative to plain water, which has been attributed to a maturation of the salt taste apparatus. Other evidence suggests, however, that dietary experience may also be involved in the development of salt liking. It was recently found that 2- to 6-month-old infants fed starchy foods, which likely are high in salt, show an elevated salt preference compared with infants not fed starchy foods and that this difference persists until at least 3 to 4 years of age.[25, 26] Another line of evidence that derives from individuals depleted of sodium early in development also implicates early experiences in modulating salt preferences (reviewed in Leshem and Beauchamp and Cowart). Thus, there is tantalizing evidence that early developmental events, perhaps resembling imprinting, have long-term influences on salt taste preferences. However, more research, in both animal models and in humans, is needed before definitive conclusions can be made about this important issue.
In summary, it is likely that both physiological maturation and specific dietary experiences impact salt preferences in infants and children. The influences of these early experiences, occurring during sensitive periods that may underlie imprinting-like processes, could have profound and long-term impacts on the extent of a person's liking for salt. This concept has important implications for strategies to reduce salt intake in the population.
Human salt preference: role of adult experience
A number of studies have demonstrated that by the time a child is ≥4 years of age not only do they exhibit a strong preference for salty foods compared with those same foods without salt, but this preference also exceeds that of adults. That is, children prefer higher concentrations of salt in food than do adults. These data suggest there are factors responsible for a relative decline in salt preference in adults, and one potential mechanism for this reduction is an adaptation to what is familiar. In support of this hypothesis, a number of studies have demonstrated that when an individual is abruptly placed on a lowered-sodium diet, preferences for salt shift downward such that the concentrations of salt in food previously perceived as optimal thus taste too salty and lower concentrations that were previously not sufficiently salty become preferred.[29-31] Although there is considerable variation across studies, the time that it takes for this shift to occur is likely several weeks at a minimum. Opposite effects have been reported for increasing salt intake in food, suggesting that the preferred level of salt is plastic and depends to some degree on what is familiar.
There are two strategies, which are not mutually exclusive, for reducing salt intake in the population. One is technological, in which researchers would develop salt taste substitutes or enhancers that, when added to lowered-salt foods, would render those foods equally salty and palatable. This approach would benefit from further understanding of the salt taste mechanisms because this knowledge could be put to use in the search for such molecules; at present, none exist that are satisfactory (see Henney et al. for a review). Moreover, because salt has such varied functions in foods, as discussed earlier, any substitutes or enhancers would need to be supplemented with compounds that have these nonsalty attributes. Much more needs to be understood about these mechanisms as well.
The second strategy would take advantage of the behavioral effects, discussed above, when individuals adapt to a reduction in their sodium intake. Recommendations focus on a gradual reduction in salt intake, with the assumption that this change would be almost unnoticed and that, over time, would result in a shift downward in optimal levels of salt in foods across the population. There are, however, no studies directly testing this assumption. Over the longer term, we have argued that experiences in infancy and childhood may be particularly important in setting salt preference levels. However, few studies have directly examined the role of early exposure to salt in children, which is a priority area for future research (see Henney et al.).
Assessing Sodium in the Us Food Supply: Methods and Measures
Depending on gender and age, adult Americans consume between 2,395 mg and 4,476 mg of sodium per day. As a frame of reference, 2,300 mg of sodium is the equivalent of 5.84 g of sodium chloride or about 1 teaspoon of table salt. The 2010 Dietary Guidelines Advisory Committee set a long-term goal for sodium consumption to be reduced to 1,500 mg per person per day.
Sodium across the food supply
Compliance with the 2010 DGA will require major shifts in consumer behavior and a profound modification of the US food supply. At this time, there is no specific guidance as to whether sodium reduction targets should apply to specific food categories or to the entire food supply as a whole. Several studies, based on the sodium content of Australian foods, noted that the food groups highest in sodium content were sauces and spreads and processed meats. Cereals and cereal products as well as vegetables and fruits were lowest in sodium. However, measuring sodium content in milligrams per 100 g does not take into account either portion size or the likely frequency of consumption. Among food products targeted for reformulation by the UK Food Standards Agency were brown table sauces, such as Worcestershire sauce.
Measures and metrics used to assess sodium sources in the everyday diet must be weighted by purchases or by frequency of consumption. An analysis of the sodium content of foods in the United Kingdom obtained sodium values (mg/100 g) weighted by annual purchases for all food categories known to be major contributors to sodium intake. Using this purchase-weighted approach, researchers concluded that the major sources of dietary sodium to food purchases were table salt, processed meats, breads and bakery products, dairy products, and only then sauces and spreads. They concluded that sodium reduction ought to be targeted to a small number of food categories and to the products sold in the highest volumes. Along these lines, a 2012 report presents a model for reducing salt intake by 0.6 to 1.0 g/d in Europe through sodium reductions in bread. In this model, sodium is replaced with potassium salts, reducing sodium by 30% and lowering the sodium/potassium ratio as well.
Sodium and food intake
An analysis of the chief sodium sources in American diets was conducted for a presentation titled “Sodium, potassium and calories: Can we successfully meet dietary guidelines?” delivered at the American Dietetic Association 2011 Food and Nutrition Conference and Expo (Drewnowski A, unpublished data). It was performed using two federal databases: the US Department of Agriculture (USDA) Food and Nutrition Database for Dietary Studies (FNDDS 1.0) and the National Health and Nutrition Examination Survey (NHANES) database. Analyses were conducted on 4,176 foods and beverages aggregated into 9 food groups, 48 subgroups, and 197 categories. The mean, median, standard deviation, and range of sodium values were calculated for food groups based on USDA food code prefixes (1, 2, and 3 digits). Foods not consumed by NHANES participants, duplicated foods, and baby/toddler foods were excluded.
Based on sodium content per 100 g, items that were highest in sodium were as follows: processed meats, seafood, bacon, processed cheese, and salad dressings (Figure 1). However, many such foods are typically consumed in portion sizes well below 100 g. The FDA definition of portion size is based on reference amounts customarily consumed, and these vary from 15 g for bacon to 240 g for milk. Values for frozen dinners are higher still. When sodium content was converted from 100 g to serving size, different food groups were at the top of the list (Figure 2). Meats, vegetables, grains, and beans were then placed above sauces and spreads.
The frequency of consumption of different sodium-containing foods is vastly unequal, resulting in some foods with high sodium content that are infrequently consumed, being only minor contributors of sodium to the diet, and vice versa. Therefore, the total sodium load, weighted by frequency of consumption, ought to be taken into account. Such an analysis was performed using dietary intake data for 4,413 adults (aged ≥ 20 years) from NHANES 2001–2002 with complete 24-h recall information. Children and adolescents, pregnant women, and individuals reporting low/high energy intake were excluded. The estimated amounts of sodium contributed by the different food groups were calculated based on reported frequency of consumption (Drewnowski A, unpublished data).
The chief sources of sodium in the US food supply were as follows: grain mixtures, mainly grain, pasta, or bread; processed meats, including frankfurters, sausages, and lunchmeats; white breads and rolls; and dishes made with meat, poultry, and fish. In general, breads and meats were the principal contributors of dietary sodium, which is a different picture than the one obtained using sodium content per 100 g.
The 2010 proposed US guidelines for sodium are 1,500 mg per person per day for vulnerable population segments (people ≥ 51 years, African Americans of all ages, and anyone with hypertension, diabetes, or chronic kidney disease), and 2,300 mg for all others. There is some question as to whether the 2010 DGA can even be met at that level of sodium restriction. For example, the guidelines may not be feasible for persons <50 years of age or those with high energy intakes. Food pattern modeling analyses based on linear programming will help determine whether the low-sodium dietary guidelines can be met using any combination of foods in the current US food supply. Another question is whether the low-sodium dietary guidelines will require drastic changes in consumer behavior. For example, diets that are adequate in nutrients yet low in sodium can be achieved, in principle, using high amounts of fruit juices, nuts, and seeds and virtually no grains and meats. Compliance with the proposed guidelines may require not only major behavioral changes but also a profound modification of the US food supply.
Further analyses are required to determine whether the sodium target is compatible with the USDA food plans, which are the mainstay of food assistance. Future analyses also must determine whether the sodium target goals will be more readily achieved given a 10% across-the-board reduction of sodium content in the US food supply.
Considerations Regarding the Reduction of Sodium in Processed Foods
Interest in the reduction of sodium in processed foods has never been higher among consumers, health professionals, and the food industry. New York City is conducting a National Salt Reduction Initiative that has established targets for sodium reduction of 62 categories of packaged foods and 25 categories of restaurant foods to be implemented over the next 2 to 4 years. This program is modeled after a similar program in the United Kingdom. More importantly, the Institute of Medicine recently recommended an aggressive strategy designed to reduce the sodium content of the US diet to the amount recommended in the 2005 DGA. The 2010 Dietary Guidelines Advisory Committee subsequently proposed a maximum daily sodium intake of 1,500 mg/day.
The food industry has responded assertively to requests for lower-sodium products and many large manufacturers have announced plans for reductions of 10% to 25% over the next several years. Increasing numbers of such products have been introduced, and approximately 7.5% of foods sold in the United States made sodium-related claims in 2006 and 2007.
Consumers are beginning to respond to the availability of lower-sodium foods. A 2008 survey by the American Dietetic Association showed that such products rated 3.7 on a 5-point scale of importance among US consumers; however, more than half of the survey respondents stated that they have not changed their consumption of such foods. A perceived lack of taste is the most important barrier for increased use of such foods, and a 2010 report by Food Navigator-USA.com concluded that only products that deliver on consumer taste expectations will survive in the marketplace. This observation is consistent with the fact that a major soup manufacturer added salt back to a variety of lower-sodium products in 2011 due to lack of acceptance by consumers.
Sodium and hypertension
The most frequently cited benefit of reduced sodium intake is lower blood pressure. Authors of the 2005 DGA and many meta-analyses and review papers have concluded that dietary sodium restriction lowers blood pressure in most people – especially those with mild to moderate hypertension.[42-46] However, the most appropriate public health strategy to lower blood pressure is still controversial; especially because weight loss and reduction of excessive alcohol consumption are known to be effective.
McCarron et al. observed that sodium intakes (determined by 24-h urine collections) of more than 6,300 residents of the United Kingdom between 1984 and 2008 fell into a relatively narrow range (approximately 135–163 mmol/day). The authors contend that such data suggest that sodium intake is tightly regulated by physiological mechanisms regardless of its concentration in the diet, and that public health initiatives designed to lower intakes of this nutrient by altering the food supply are destined to fail. In addition, Appel et al. demonstrated that the Dietary Approaches to Stop Hypertension, or DASH, diet is more effective at lowering blood pressure than sodium restriction. This diet, which includes generous amounts of fruits, vegetables, and low-fat dairy products, has been recommended for a variety of health benefits in addition to blood pressure reduction and is considered by some to be a preferable alternative to sodium restriction.
The role of salt in food
Despite the controversy regarding public health strategy, a variety of practical challenges must be overcome to ensure that lower-sodium foods will be purchased and eaten by consumers. Palatability is the most serious barrier to the development of appealing lower-sodium foods. This challenge will be formidable if the new IOM recommendations are to be achieved because a reduction in mean sodium intake of 50% among US women and 67% among men would be required to achieve the goal of 1,500 mg/day. Sodium is a powerful contributor to the palatability of foods because it reduces objectionable flavors (e.g., bitterness) while enhancing those perceived as pleasant (e.g., umami, sweet). This ability makes foods such as cheese taste “cheesier” and vegetables taste less bitter without necessarily making them taste salty. On the other hand, the salty taste contributed to some foods (e.g., savory snacks) can also be very important.
Unfortunately, there are no alternatives for salt that mimic its sensory properties without contributing objectionable characteristics. The development of a suitable salt substitute has been hampered by the fact that the salt receptors on the tongue respond only to sodium, lithium, or potassium. Lithium chloride is toxic. Potassium chloride is the most widely used salt substitute but it imparts a bitter taste that is difficult to mask. The FDA acknowledged the technical difficulties pertaining to the development of lower-sodium foods when it decided not to lower the limit for the sodium content of products eligible to bear the “healthy” claim from 480 to 360 mg/serving.
Sodium chloride also contributes to the safety of food products by helping to maintain microbiological stability. This property is important for foods such as bacon, bologna, deli meats, processed cheeses, smoked fish, cheese spreads, poultry cuts, pickles, olives, butter, hard cheeses, and salad dressings. Sodium chloride is superior to other salts in its ability to foster microbiological stability. For example, Barbut et al. demonstrated that sodium chloride is more effective than potassium chloride or magnesium chloride at inhibiting the production of Clostridium botulinum toxin in frankfurters.
Finally, table salt contributes to the functionality of a wide variety of foods. Examples of this property include the following: firm texture in processed meats and hard cheeses; binding strength in meats by extracting proteins; tenderness of cured meats; gluten strength for uniform texture and grain in bread; color development in meats such as ham, bacon, and frankfurters; golden color of bread through caramelization; fermentation control in sauerkraut and fermented sausages; and control of ice-crystal formation in frozen products.[50, 52]
In conclusion, it is clear that while human preference for sodium is well-preserved, the mechanism is not yet clearly understood. Due to health considerations, sodium reduction is a major priority for a variety of stakeholders, including government policy makers and food manufacturers. The food industry has made significant reductions to the sodium content of its products on a voluntary basis, and has pledged to continue this initiative. Consumers have expressed interest in such foods, but their success will depend on taste and other quality factors. It is also important to consider amount and frequency of consumption of products when initiating dietary changes, and it will be necessary to both educate the consumer as well as work with industry to reduce sodium content in the food supply. Controversy still exists regarding the best strategy to lower blood pressure, and some experts believe that physiological regulation of sodium intake will undermine public health strategies based on alteration of the food supply. The most serious obstacle to the development of commercially successful lower-sodium foods is palatability, followed by a variety of factors in the area of food safety and functionality.
This review is based on information presented at the Experimental Biology meeting in Anaheim, CA, April 2010 and was sponsored by the North American Branch of the International Life Sciences Institute's Sodium Committee.
The authors were provided with an honorarium for participating in the seminar and for contributing to this article by the Sodium Committee of the North American Branch of the International Life Sciences Institute.
Declaration of interest
The authors have no relevant interests to declare.