Explaining variability in sodium intake through oral sensory phenotype, salt sensation and liking
Introduction
Of the 71 million Americans with some form of cardiovascular disease, an estimated 65 million have hypertension [1]. Nearly one-third of deaths globally are attributed to cardiovascular diseases, and about 23% of these deaths relate to hypertensive and other heart conditions [2]. The link between dietary sodium and hypertension is well established [3] and dietary modification is a primary step in hypertension risk reduction. Yet, in spite of extensive public health education campaigns, sodium consumption exceeds recommendations. For example, according to the 2005–2006 Nutritional and Health Examination Survey Data, 20 to 29 year old men consume nearly double the recommended sodium intake (< 2300 mg/day) while women consume 135%. [4]. Intake of sodium above recommended levels likely comes from consumption of processed foods and beverages [5], [6] to which sodium salts have been added for flavor enhancement (e.g., saltiness, blocking unpleasant sensations, increasing sweetness) [7], [8] or functional reasons (e.g., preservation, moisture control, texture). Since consumers report that taste is an important determinant of food selection [9], the present study examined whether normal variation in taste and oral sensation influenced salt sensation sufficiently to affect liking and consumption of high-sodium foods.
The perceived intensity of sodium chloride varies such that a specific concentration required to elicit weak saltiness in one individual may be strongly salty to another. Critically, these differences are not merely the result of differences in response bias, but appear to result from underlying variation in taste function. The best-studied phenotypic marker of variation in taste and oral sensation is the perceived bitterness of propylthiouracil (PROP) [10]; some additional markers include the density of taste papilla on the tongue tip (fungiform papilla) and thermal tasting [11]. Differences in the perceived bitterness of PROP have repeatedly been shown to associate with the saltiness of simple salt solutions [11], [12], [13] and beef broth [14] when using methods that allow for valid across subject comparisons [15]. In beef broth, those who taste PROP as more bitter are able to detect smaller changes in salt concentration [14]. One prior study failed to find PROP effects on perceived saltiness of solid foods [16]; however, PROP phenotype was defined as the ratio of PROP bitterness to NaCl saltiness, which has limited validity for examining PROP effects on salt perception, as the phenotype was confounded with the outcome measure. In addition to behavioral measures, greater density of fungiform papillae explains heightened saltiness of salt solutions on the tongue tip [17], [18], but may have less impact on whole mouth saltiness [12]. Thus, the question of whether commonly studied oral sensory phenotypes influence the perceived intensity of sodium chloride in foods remains unclear. Here, we address this knowledge gap by examining taste phenotype (perceived bitterness of PROP and number of fungiform papillae) and salt sensation/liking in aqueous solution, in chicken broths with increasing amounts of added sodium chloride, as well as sampled high-sodium foods.
The hedonic response to saltiness in humans results from a complex interplay of physiological, cultural, and environmental factors that influence avidity for and access to high-sodium foods. Critically, humans are different from other animals in that there is little evidence for a general ‘salt appetite’ [19]. That is, humans consume salt for pleasure and not to meet physiological need. Thus, our goal here was to focus specifically on variation in salt sensation in healthy adults and the extent to which this variation may influence the liking for the sensation of salt in aqueous solution, broth and perceptually complex food products. As stated above, we also examined markers of variation in taste and oral sensation that are hypothesized to influence the development of food preferences (e.g., [20], [21] but also [22]) .
In a liquid food such as a broth, the relationship between liking and sodium concentration forms an inverted U: liking is initially low before rising to a peak and subsequently falling, although the shape of the function varies across individuals [23], [24]. Differences in perceived intensity may affect the sodium chloride concentration required to achieve maximal liking. At higher concentrations, perceived intensity from salt would be comprised by both salty taste and irritation [25], although it is not clear whether individuals can reliably partition out the relative contributions of these qualities in the overall percept elicited by concentrated sodium chloride. In a previous study, those tasting PROP as more bitter (supertasters) showed greater hedonic response to changes in salt level in beef broth, preferring the addition of smaller amounts to the broths than did the nontasters [14]. Unfortunately, the study was confounded by sex differences in the taster groups, which could influence sodium chloride hedonics — only 8% of the supertasters were male versus 25% of the nontasters and 50% of the medium tasters. Here, in a cohort where the distribution of PROP bitterness did not differ between men and women, we tested a) whether oral sensory phenotype influenced perceived intensity enough to shift the concentration in broth where peak liking occurs and b) if the relationship between changing concentration and hedonic responsiveness varied by oral sensory phenotype.
Some reports suggest sex hormones may influence salt preference [26], [27], [28] although results in humans are inconsistent (see [19]). In rodents, estrogen present during development may moderate taste responses [26] with females being less averse to high concentrations of sodium chloride in solution [29]. In humans, changing hormone levels associate with changes in salt sensation and hedonics; a longitudinal study across pregnancy [30] shows that saltiness of aqueous sodium chloride falls with a concurrent reduction in the unpleasantness from 1st to 3rd trimesters. Likewise, preferred level of salt on popcorn varies with the phase of the menstrual cycle [27]; conversely, preference does not differ across prepubescent girls and boys [28]. However, apparent differences in salt preference associated with sex hormone fluctuations could be the result of cognitive control of eating (dietary restraint) as show by Kanarek et al. [31]. The present study characterizes differences in salt sensation and hedonics across males and females who do not report an excessive level of dietary restraint on eating.
A substantial body of literature supports that food liking and preference are strong predictors of intake (e.g. [32], [33]). Specific to salt, a small majority of studies report positive associations between salt hedonics and sodium intake [34]. Early work from the Pangborn laboratory found consistent trends between hedonics and intake in a small sample of college students. Individuals who habitually consumed more sodium added more salt to reach optimal saltiness in tomato juice [35] and in beef broth [24] and the concentration that elicited maximal liking also correlated with intake [24]. Shepherd and colleagues found that individuals who consume more sodium prefer greater salt concentrations in tomato soup [36], although they caution that preference may be more tightly linked to discretionary salt usage rather than total sodium intake [37] because many important sources of dietary sodium are not salty [38]. Recently, Kim and Lee reported associations between elevated salt thresholds, elevated liking for salt in broth, and elevated consumption of salty foods among Korean adolescents [39]. With a more distal outcome of sodium intake, Contreras [40], using data from Moskowitz and Abrahmson, showed the inverted U is shifted to the right for hypertensive individuals (i.e., peak liking occurs at a higher concentration) as compared to normotensive individuals, while Mattes [41] did not find mean differences in salt preference across blood pressure groups.
Some studies fail to find associations between salt hedonics and sodium intake: the lack of consensus may be due to insensitivity in methods used to assess sodium intake [34]. Most prior studies estimate intake using un-validated questionnaires or single 24-hour urinary collection. Notably, the assumption that methods from analytical chemistry are superior for assessing intake should be tempered by two factors. First, a large variation in intake across days makes any single point estimate suspect. More critically, excreted sodium may differ substantially from estimated intake, even when intake estimates are based on analysis of the foods actually consumed [42]; this is consistent with evidence that the rate of ion excretion is not stable even when intake is constant [43]. The present study builds on prior work by associating salt sensation with multiple measures of sodium intake: quantitative food frequency, five non-consecutive 24-hour food records (see [44]), and liking for high-sodium foods, which may be an intermediate step between sensation and intake [45] and reflect habitual intake patterns [46], [47].
In summary, the present study examined variability in salt sensation and hedonics and the extent to which this variability was associated with consumption of high-sodium foods. Specifically, do phenotypic measures of variation in oral sensation explain differences in perceived saltiness and hedonic response across diverse stimuli including aqueous solutions and solid foods? This is conceptually consistent with our working hypothesis that variation in taste and oral sensations influence food liking and disliking, and ultimately dietary intake. We aimed to examine relationships between salt sensation, liking and intake in normally nourished adults and thus distinguish our work from the investigation of sodium appetite in response to dehydration and thirst (e.g., [48]). Our general findings were that variation in perceived saltiness and liking across multiple foods were linked to sodium intake, and at least some of this variation in perception and hedonics was related to two commonly studied oral sensory phenotypes. PROP bitterness, was associated with differences in salt sensation in aqueous solution, broth, and foods for which saltiness is a predominant sensation (e.g., pretzels and potato chips) or in cheese where salt serves to block bitterness. Those who tasted PROP as most bitter reported greater changes in perceived saltiness with changes in salt concentration. Salt sensation was linked to liking in these foods with predominant saltiness; oral sensory phenotype associated to the hedonic responses indirectly through salt sensation. Sex differences in saltiness or liking for high-sodium foods attenuated the oral sensory phenotype effects. Women reported greater liking for moderate sodium chloride concentrations in either aqueous solutions or chicken broth. Evaluated via Structural Equation Models, oral sensory phenotypes were associated with variance in intake of high-sodium foods indirectly — PROP effects on intake were mediated via salt sensation and liking while fungiform papilla number was related to sodium intake via liking of high-fat foods that are also high in sodium, rather than saltiness per se.
Section snippets
Subjects and procedure
Subjects came from an on-going observational study to examine relationships between oral sensation and dietary behaviors, similar to previous reports [49], [50]. The sample included reportedly healthy males and females (n = 87; 42 F), who ranged in age from 20–40 years. The majority (63 of 87) had a normal body mass index (BMI; weight (kg)/height (m2) from 19–24.9), while 23 were overweight (BMI 25 to 29.9) and 3 were obese (BMI > 30). Men were more likely than women to fall in the overweight/obese
Taste phenotype
The sample showed diversity in taste phenotype. When categorized by perceived bitterness of 3.2 mM PROP, there were 21 nontasters (gLMS ≤ moderate), 37 medium tasters (> moderate and < very strong) and 29 supertasters (≥ very strong). Females and males did not differ significantly in the mean or distribution of PROP ratings. Fungiform papillae per 6 mm area (range 11 to 42) correlated significantly with 3.2 mM PROP bitterness (r = 0.37, p < 0.001). For categorical analyses, average papillae number was
General findings
Multiple physiological, socio-cultural, economic and environmental factors influence the ingestion of sodium and the study of these factors are of great interest for health and wellness. The present study focused specifically on individual differences in salt sensation and the relationship with salt sensation, liking for high-salt foods, and sodium consumption in a sample of reportedly healthy adult men and women who were mostly of normal weight and who did not report excessive levels of
Acknowledgements
The project was supported by the USDA Hatch Project CONS00827 and NIH Institutes of Deafness and Communication Disorders grant number DC00283. The authors thank Megan Philips and Julie M. Peterson for collecting these data.
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