Taste Perception in Three Individuals on a Low Sodium Diet

Appetite 1981, 2, 67-73

Taste Perception in Three Individuals on a low Sodium Diet MARY BERTINO Monell Chemical Senses Center, Philadelphia

G. K. BEAUCHAM P Monell Chemical Senses Center and Department of Otorhinolaryngology and Human Communication University of Pennsylvania

D. R. RISKEY Monell Chemical Senses Center

K. ENGELMAN Clinical Research Center, Hospital of the University of Pennsylvania

There is little information on the effect of dietary sodium on taste responses to sodium in humans. Since individuals with hypertension are routinely suggested to maintain a low sodium diet, knowledge of effects of changes in dietary sodium on taste is important. Three subjects were placed on a low sodium diet for three and a half weeks. Detection thresholds for salt and sucrose solutions, and sensory and hedonic responses to salt in soup and sucrose in Kool-Aid were monitored before, during, and after placement on the diet. Detection thresholds for salt and sugar solutions, and intensity and pleasantness ratings of sweetened Kool-Aid were unaffected by dietary manipulation whereas intensity and pleasantness ratings of salt in soup were altered. While the subjects were on the low sodium diet, highly salted soup was judged to taste less intense and more pleasant compared with pre- and post-diet periods. These data parallel results obtained with sodium deficient rats.

One factor that influences responsiveness to salt is the amount of sodium available to the organism. Sodium deficiency in rats produced either by adrenalectomy or by low sodium diets (Richter, 1956) raises the acceptability of salt solutions, particularly high concentrations which normal subjects reject (Contreras, 1979). Addison's disease is a disease where the adrenal cortex is damaged and the ability to retain sodium is impaired. Some patients with Addison's disease crave salt (Liddle, 1974; Wilkins & Richter, 1940). Section of the taste nerves eliminates the adrenalectomized rats' ability to maintain a high salt intake when given a choice between saline and water (Richter, 1956). Thus, salt intake apparently increases with need and taste is known to play an important role in this increased intake. One possible mechanism increasing sodium intake during deficiency derived from the animal literature is that deficiency may alter the taste receptors in such a way to make them less sensitive to supra threshold concentrations of salt (Contreras, 1979). - - - - - - - - - - - - - ------

This research was approved by the Committee on Studies Involving Human Beings of the University of Pennsylvania and, the Clinical Research Advisory Committee at the Hospital of the University of Pennsylvania. Support for this research was provided by the Clinical Research Center (CRC), NIH-5-M01RROO040 and USDA 59-32U4-0-3. We appreciate the technical assistance of Barry Fabius and Diane Wang, the dietician at the CRe. We thank Campbell soups for providing us with the low sodium vegetable soup. Dwight R. Riskey is now at General Foods Corporation, Technical Center, Tarrytown, NY 10591, U.S.A. Reprint requests should be sent to Dr Mary Bertino, Monell Chemical Senses Center, 3500 Market Street, Philadelphia, PA 19104, U.S.A. 0195-6663/81/010067 +07 $02'00/0

(t) 1981 Academic Press Inc. (London) Limited

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The performance of adrenalectomized rats did not differ from controls in an operant task where reward was contingent on discriminating very low concentrations of salt solutions from water. When the strength of these solutions was increased, adrenalectomized rats did not perform as well as controls, as if they were less sensitive than the controls to the high salt concentrations (Morrison, 1980). When given the opportunity, sodium replete rats and humans continue to choose to ingest salt. This supplemental intake is thought to be in response to sensory pleasure from the taste of salt. Yet little is known about what factors influence salt intake in nondeprived organisms since most studies have been conducted with severely deprived groups. Knowledge of the effect of alterations in levels of dietary salt within the nondeficient range upon salt taste is of clinical importance. Patients with essential hypertension are frequently placed on low sodium diets as part ofthe therapy regimen in blood pressure management. This treatment necessitates that the patient forego a source of sensory pleasure. The ease with which a person is able to alter his/her dietary habits may be determined in part by changes in the sensory properties of salt. If an individual becomes more sensitive to the taste of salt sometime after initiation of a low sodium diet, it might be expected that the diet may be easier to maintain. Unlike severe sodium deficiency where salt preference increases, there is anecdotal evidence that sometime after placement on a low sodium diet, salt appetite decreases (Dahl, 1958; Stephansson, 1946), and patients have reported that normally salted foods, which they previously preferred, now taste "too salty". It is not known if this is a reliable effect or what other sensory changes may result. The following study is an initial step in the characterization of the effects of a low sodium diet on salt taste in aqueous solutions and in a real food. METHOD

Three healthy university student volunteers scaled intensity and pleasantness of soups varying in Na concentration and soft drinks varying in sucrose concentration. Threshold measurements for NaCI and sucrose were also made. Baseline measures were obtained twice during a two week period while the subjects were on their normal, ad lib. sodium diet. Baseline measurements of urinary sodium and creatinine excretion were also collected at this time. Baseline results were compared (a) with evaluations made during a J~ week period in which subjects followed a restricted (low) sodium diet and (b) with a subsequent recovery period during which subjects resumed their normal eating patterns in which sodium was not restricted. Stimuli for Rating and Threshold Procedures

Stimuli for the rating procedure were soups to which reagent grade NaCI had been added to produce nine concentrations of Na ranging from 0·07 to 1·0 Min equal log steps. In order to ensure that the results obtained would reflect taste interactions with real foods, soup and Kool-Aid were used as the diluents. Campbell's low-sodium (containing approximately 0·01 M Na) vegetable soup was used. Vegetables were extracted from broth by straining and NaCI was added to produce the concentrations tested. Uncarbonated beverages were prepared with nine concentrations of reagent grade sUcrose ranging from 0·7 to 1·5 M in equal log steps. Cherry flavored Kool-Aid unsweetened soft drink mix (General Foods Corporation) was used as flavoring. Each

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liter of beverage contained 3·5 g of flavoring. Aqueous solutions for evaluating threshold levels of detection ranged downward from 0·1 M for N aCI and 0·3 M for sucrose in equal log steps; each concentration was reduced from the next higher concentration by a factor of 0·77. Approximately 10ml of each solution was presented in one-ounce plastic cups. Soups were served at 57~C; all other stimuli were served at room temperature (approximately 21 C). Solutions were refrigerated during storage periods and were never used after more than 5 days storage. Water used throughout the investigation was charcoal filtered and deionized to a resistance of at least 18 MQ. Diet

Once the low sodium diet was initiated, subjects were provided with food by the Hospital of the University of Pennsylvania Clinical Research Center (CRC). Meals were specially prepared by the Clinical Research Center staff to provide approximately 75 mEq of sodium (1· 73 g) per day. Snacks were provided by the CRC and subjects were permitted to drink beer which contains 7 mgm sodium per 100 g beer. Subjects remained on the diet for 24 days, after which sensory testing continued for an additional 14 days. Four times during the study, once before and three times after the subjects went on the low sodium diet, they were required to provide a twenty-four hour urine sample. These samples were evaluated for sodium and creatinine content to test for compliance with the diet. The timing of each urine collection was unannounced. Blood pressure and body weight were recorded periodically while subjects were on the diet. Rating Pr6cedure

Judgments of soups and soft drinks were made in separate I-h test sessions. Each subject judged the intensity (i.e. saltiness or sweetness) and pleasantness of five complete sets of the nine concentrations. An initial set ofthe nine stimuli was presented for practice and was not tabulated with the remaining judgments. These initial nine trials were not identified to the subjects as practice. Stimuli were presented in random order with the restriction that each of the nine concentrations in one replicate was presented before any ofthe nine concentrations comprising the next replicate. Ratings were made using a 9-point category scale ranging from 9 (extremely salty or sweet) to 1 (no saltiness or sweetness whatsoever) and from 9 (extremely pleasant) to 1 (extremely unpleasant). Subjects were required to always report judgments of intensity, then pleasantness for each stimulus. A standard sip and spit procedure was employed in which subjects sipped all of the stimulus contained in the cup, expectorated it, verbally reported judged saltiness or sweetness and pleasantness, and finally rinsed thoroughly with water in preparation for the next stimulus. Trials were self-paced with most subjects completing the taste session within 50 min. An additional test of preference, the choice selection task, was conducted at the end of each testing session. All nine concentrations were presented to the subject at one time in random order. Subjects were instructed to taste and retaste the nine samples as many times as necessary, then to select the most pleasant tasting sample. Threshold Procedure

Threshold sensitivity was measured using a staircase procedure in which subjects were presented a randomly selected stimulus (i.e. a solution containing either NaCI or

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sucrose at any concentration within the range tested) or water. A sip and spit procedure was employed (see above) and the subject reported whether or not the solution contained a tastant. Stimuli containing sodium chloride, sucrose and no tastant were presented in random order and with approximately equal frequency during the session. Whevever a tastant was correctly detected (but not necessarily correctly identified) that tastant was reduced in concentration by one step. When a stimulus was not detected, the following presentation of that tastant was the next higher concentration in the series. The procedure continued for both tastants until the direction of the staircase reversed at least twelve times for each tastant. The threshold concentration was then concluded to be the most frequently presented stimulus. Reports oftastes of blank trials were recorded as a measure of response bias (i.e. the tendency to incorrectly report a taste for stimuli containing only water). The entire process lasted from 40 to 75 min. Each of the three tasting sessions (i.e. intensity and pleasantness for soups, intensity and pleasantness for soft drinks, thresholds for NaCI and sucrose) were administered twice during the baseline period, three times during the diet period and twice during the recovery period. Tests of the same type were spaced at least one week apart. Subjects were tested individually. Subjects

The three subjects were males, 18- 23 years of age, selected from a larger group of student volunteers from the University of Pennsylvania. Subjects were screened for poor health, food aversions and willingness to stay on the diet. Subjects were informed and consented to being placed on low sodium diets. They were not informed as to the specific purpose of the investigation. The subjects were paid for participation in the study. RESULTS

Due to the small number of subjects in this study we present the data for each subject separately. There was substantial between-subject variation in the reporting of false positives in the detection threshold procedure. There was no consistent influence of diet either on report offalse positives or on the variation in thresholds for either sucrose or salt during the experiment. Across the entire experiment, detection thresholds for sodium chloride averaged 5·4mM (±0'080) and for sucrose averaged ll'OmM (±0·20). Soups with the higher concentrations of sodium (0'26-0'71 M) were rated by each individual as tasting less intense when they were on the low sodium diet than when they were either in the pre- or post-diet period (Figure 1). With the exclusion ofO'26M Na, these same soups were rated by each individual as tasting more pleasant when they were on the low sodium diet. Consistent with the pleasantness ratings in Figure 1, diet appeared to also influence the choice selection tasks of the soups. All three subjects preferred higher concentrations during the low sodium diet. The preferred salt concentration increased from an average of 0·27 M(± 0·04) to O' 36 M(± 0·06) while the subjects were on the low sodium diet. Return to a diet permitting free use of salt resulted in a drop in preferred concentration to an average of O· 22 M (± 0'02). There were no consistent changes in intensity ratings of Kool-Aid containing varying concentrations of sucrose during the experiment. The only consistent change in hedonic ratings of Kool-Aid was that all three subjects assigned higher pleasantness ratings to the lowest concentration of sucrose as the experiment proceeded.

71

TASTE PERCEPTION ON A LOW SODIUM DIET

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FIGURE 1. Mean intensity and hedonic ratings for salt in low sodium vegetable soup lor each individual during the low sodium diet period (0) and ad lib . sodium periods pre-diet and post-diet (.). Each pointin the low sodium curves represents an average of three series of judgments. Data points in the ad lib . sodium curves each represent an average of two series of judgments per subject. The dotted lines represent the averages of the pre-diet and post-diet periods.

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All three subjects lost weight while they were on the low sodium diet, with an average loss of 4·2lb. The urinary sodium/creatinine ratio dropped in all the individuals with an average of 2·36 (±0·39) just prior to placement on the diet to 0·69 (± 0·07) at the end of the diet. Urinary excretion of sodium dropped in all three with an average of 164 (± 24·3) mEqjl to 53 (± lO·O)mEqjl. The ratios and total sodium excretion values were low throughout the diet period. Blood pressure was unaffected by the diet.

DISCUSSION

Although the sample size was small and the duration of the low sodium diet brief, the data suggest that a restriction in dietary sodium for less than one month alters the perceived intensity and the pleasantness of the taste of salt. Alternative hypotheses to explain these data, such as weight loss, monotony of the hospital diet, the subjects' own hypotheses or expectations about the effects of the diet, or the effect of repeated testing on taste responsiveness appear unlikely for the following reasons. First, weight loss has not been shown to influence either the rated intensity or pleas an tness of the taste of salt (Rodin, Moskowitz & Bray, 1976). Second, a monotonous diet could be expected to increase the pleasantness of strong tastes in general while the present data show an

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effect specific to salt but not sucrose. Third, when debriefed, the subjects' hypotheses concerning the dietary effects on pleasantness ratings were varied and not parallel to the experimental results; importantly, they had no clearly expressed hypotheses concerning the intensity ratings. Finally, it seems unlikely that repeated testing could have induced first a decrease and then an increase in the intensity judgments ofthe same solutions. The source of the changes in salt taste then, was probably the dietary manipulation. Some question remains as to whether the changes in taste response to sodium chloride were due to the low sodium in the experimental diet or a change in some other dietary constituent. It has been demonstrated that animals on high fat diets drink less salt solution than animals on high carbohydrate diets (Smith, 1979). Without dietary histories, it cannot be determined if the hospital diet substantially altered the intake of carbohydrates and fats and influenced the taste of salt. The obtained threshold measures are in general agreement with previously published values (e.g. Amerine, Pangborn & Roessler, 1965; Grzegorczyk, Jones & Mistretta, 1979). No dietary effect on the detection threshold of sodium chloride was observed. These data appear to conflict with those collected by Yensen (1958) who observed decreased thresholds in two subjects on low sodium diets and those of Henkin (1967), who observed decreased thresholds in patients with Addison's disease. The variation in results could be due to a number of procedural differences. Yensen's low sodium diet was quite extreme providing only approximately 75 mgm sodium per day. This could have produced a substantial reduction in salivary sodium (McCance, 1938; Wotman, Baer, Mandel & Laragh, 1973). In threshold testing, Yensen presented one stimulus per minute which may have been slow enough to allow the tongue to adapt to the salivary sodium and influence the threshold obtained (Bartoshuk, 1974). The low sodium diet in the present study (1'73 g Na per day) was not nearly as extreme and may not have affected salivary sodium content. In addition, the threshold procedure we used was self-paced, with a good possibility that the subjects were water adapted. Variation in salivary sodium concentration is an unlikely cause for the observed changes in the intensity and pleasantness ratings of the soups. One would expect dietary induced decreases in salivary sodium to make the salt in the soups taste more intense. We observed changes in the opposite direction. The intensity ratings and hedonic ratings appeared to be related. Generally, when the subjects went on the low sodium diet, the intensity ratings of the high concentrations of salt solutions decreased and pleasantness ratings increased. When the subjects were removed from the diet, the ratings of the strong salt solutions increased in intensity and decreased in pleasantness (see Figure 1). The threshold and suprathreshold data compare favorably with those observed in adrenalectomized rats which are not as responsive as normal rats to strong solutions of salt (Morrison, 1980). These animals consume high concentrations ofNaCI solutions which would normally be rejected (Richter, 1956), possibly a result of a lowered sensitivity to suprathreshold levels of salt, making higher concentrations seem less intense and more pleasant (Contreras, 1979). The findings that strong solutions become less intense and more pleasant run counter to anecdotal statements concerning the effects of low sodium diets on taste (Dahl, 1958; Stephansson, 1946). If taste tests are reflective of responses outside the testing situation and if anecdotal reports are to be believed, the question remains as to how low sodium diets come to be preferred. The effects documented in the present study may be acute and indicate that one must remain on the diet longer than three weeks for the taste of low sodium foods to become more pleasant.

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REFERENCES

Amerine, M. A., Pangborn, R. M., & Roessler, E. B. Principles of sensory evaluation offood. New York: Academic Press, 1965. Bartoshuk, L. NaCl thresholds in man: Thresholds for water taste or NaCl taste? Journal of Comparative and Physiological Psychology, 1974,87, 310-325. Contreras, R. Salt taste and disease. American Journal of Clinical Nutrition, 1979,31,1088-1097. Dahl, L. Salt intake and need. New England Journal of Medicine, 1958,258, 1205-1208. Grzegorczyk, P. B., Jones, S. W., & Mistretta, C. M. Age-related differences in salt taste acuity. Journal of Gerontology, 1979, 34, 834-840. Henkin, R. I. Abnormalities of taste and olfaction in various disease states. In M. R. Kare & O. Maller (Eds.), The chemical senses and nutrition. Pp. 95-113. Baltimore: The John Hopkins Press, 1967. Liddle, G. W. The adrenal cortex. In R. H. Williams (Ed.), Textbook of Endocrinology, Pp. 233-282. Philadelphia: W. B. Saunders, 1974. McCance, R. A. The effect of salt deficiency in man on the volume of the extra-cellular fluids and on the composition of sweat, saliva, gastric juice and cerebrospinal fluid. Journal of Physiology, 1938,92,208-218.. Morrison, G. R. Measuring taste sensitivity and the effects of adrenalectomy in rats. In M. R. Kare, M. J. Fregly & R. A. Bernard (Eds.), Biological and behavioral aspects of salt intake. Pp. 127-137. New York: Academic Press, 1980. Richter, C. Salt appetite in mammals; its dependence on instinct and metabolism. In M. Autuori (Ed.), L']nstinct dans Ie Comportement des Animaux et de ['Homme. Pp. 557-629. Paris: Masson, 1956. Rodin, J. Moskowitz, H. R., & Bray, G. Relationships between obesity, weight loss and taste responsiveness. Physiology and Behavior, 1976, 17,591-597. Smith, P. A. Pressor effects offat and salt in rats. Ph.D. Thesis, Rutgers, The State University, 1979. Stephansson, V. Not by bread alone. New York: Macmillan, 1946. Wilkins, L., & Richter, C. P. A great craving for salt by a child with cortico-adrenal insufficiency. Journal of the American Medical Association, 1940, 114, 866-868. Wotman, S., Baer, L., Mandel, I. D., & Laragh, J. H. Salivary electrolytes, renin and aldosterone during sodium loading and depletion. Journal of Applied Physiology, 1973,35, 322-324. Yensen, R. Influence of salt deficiency on taste sensitivity in human subjects. Nature, 1958, 181, 1472-1474.

Received 29 July, 1980; revision 15 November, 1980