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Sweet taste and diet in type II diabetes
Physiology & Behavior, Vol. 60, No. 1, 13-18, 1996 Copyright © 1996 Elsevier Science Inc. Printed in the USA. All rights reserved 0031-9384/96 $15.00 + .00
ELSEVIER
SSDI 0031-9384(95)02242-2
Sweet Taste and Diet in Type II Diabetes B E V E R L Y J. TEPPER, .1 L I S A M. H A R T F I E L * A N D STEPHEN H. S C H N E I D E R t
*Department of Food Science, Rutgers University, New Brunswick, NJ, and ?Department of Medicine, Division of Endocrinology, Metabolism and Nutrition, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson University Hospital, New Brunswick, NJ, USA Received 2 June 1995 TEPPER, B. J., L. M. HARTFIEL AND S. H. SCHNEIDER. Sweet taste and diet in type H diabetes. PHYSIOL BEHAV 60(1) 13-18, 1996.--The relationship between sweet taste function and dietary intake was studied in 21 patients with type II diabetes mellitus and 16 age-, weight-, and sex-matched controls. Subjects rated the sweetness intensity and pleasantness of a series of beverage samples sweetened with sucrose: 1.5-24%, fructose: 1-18%, or aspartame: 0.25-4%. They also kept 7-day food records. No group differences were found in sweet taste perception, pleasantness ratings, daily energy intakes, or macronutrient composition of the diets. However, subjects with diabetes consumed less sucrose but 3.5 times more alternative sweeteners than did controls. Peak pleasantness ratings for the beverage samples were positively correlated with dietary sweetness content in the subjects with diabetes but not the controls. These findings suggest that in diabetes, hedonic ratings for a sweetened beverage were related to dietary sweetness intake rather than changes in sweet taste perception. Diabetes
Taste
Sweetness
Diet
TYPE II (non-insulin-dependent) diabetes mellitus is characterized by abnormal carbohydrate metabolism and can be accompanied by a number of pathologic conditions affecting the kidney, eye, cardiovascular, and nervous systems. Diabetes also affects taste function, with sweet taste being the most vulnerable [see (26)]. Taste thresholds (e.g., the point at which a weak solution can be distinguished from plain water) are elevated in diabetic individuals for certain simple sugars including glucose (16,23) and sucrose (1,16). Although neurological complications appear to exacerbate taste deficits (1), they are not are critical for the expression of taste changes; taste deficits are also found in individuals with diabetes in the absence of neurological involvement (16) and in first-degree relatives who show no overt symptoms of the disease (16,25). A number of questions about the relationship between taste and diet in diabetes remain unanswered. First, with few exceptions (12,15) almost all studies examining taste in diabetes have used aqueous solutions rather than actual foods (1,8,10,16,22,23,25). Laboratory solutions lack the gustatory and textural qualities of complex foods and are often viewed as "test" solutions by subjects. Real foods need to be examined to determine whether such taste changes are nutritionally meaningful to individuals with diabetes. For example, if individuals with diabetes required more sweetening agent to attain the same level of sweetness in foods, then taste disturbances could make dietary
adherence difficult to achieve. Second, although a link between taste changes and dietary habits in diabetes has often been suggested, this relationship has never been directly tested. Studies are needed that examine both the taste and diet measures in the same individuals. Third, current recommendations support the utility of alternative sweeteners in the diabetic diet and such products are well accepted by the diabetic population (2,3). However, it is unclear whether individuals with diabetes experience changes in taste for these agents as they do for some of the simple sugars (12). The present study was undertaken to resolve these issues. The first objective was to evaluate sweet taste perception and pleasantness in a fruit beverage containing various levels of carbohydrate or alternative sweeteners in individuals with type II diabetes and control subjects. The second goal was to establish the dietary patterns of these individuals and evaluate possible relationships between the dietary factors and the taste ratings. METHOD
Subjects Subjects were 21 individuals with type II diabetes (15 men, 6 women) and 16 age- and weight-matched nondiabetic controls (10 men, 6 women). Individuals with diabetes were recruited by
1 Requests for reprints should be addressed to Beverly J. Tepper, Ph.D., Rutgers University, Department of Food Science, Cook College, P.O. Box 231, New Brunswick, NJ 08903.
13
14 their physicians at the Department of Endocrinology and Nutrition, Robert Wood Johnson University Hospital, and also by local newspaper advertisement. Control subjects were senior citizens recruited from local community centers and nontechnical employees of Rutgers University. Prior to acceptance into the study, all potential subjects were screened by telephone interview to ensure that they were in good health. Only those individuals with diabetes who exhibited good control (i.e., a recent fasting plasma glucose < 200 mg/dl), had been diagnosed at least 1 year prior to the study, and had normal kidney function were allowed to participate. Informed consent was provided by each subject on the first day of the study. In addition, medical histories were reviewed for the duration of diabetes, a recent glycosylated hemoglobin value (an indicator of long-term glycemic control), and current medication use. Evidence of degenerative complications was also recorded, including the incidence of cataract, peripheral vascular disease, and peripheral neuropathies (sensory and motor combined). All procedures were approved by the Institutional Review Boards of Rutgers University and the University of Medicine and Dentistry of New Jersey.
Experimental Measures Taste stimulus. The taste stimulus was a cherry-flavored beverage (Kraft General Foods, Inc., White Plains, NY; 2.1 g cherry Koolaid base/1 deionized water). Beverage samples were prepared with five concentrations of either sucrose (1.5%, 3%, 6%, 12%, and 24%), fructose (1%, 2%, 5%, 10.2%, and 18%), or the alternative sweetener aspartame (as Equal TM, G. D. Searle Co., Chicago, IL; 0.25%, 0.5%, 1%, 2%, and 4%.; Equal" provides 35 mg aspartame/packet). A pilot study revealed that the sweeteners were equisweet at the aforementioned concentrations. A series of glucose solutions was also evaluated as a training exercise to accustom the subjects to the use of the rating scales. Glucose solutions were prepared in five concentrations (3.1%, 7%, 10.5%, 19.8%, and 34.2%) in deionized water. All percentages were calculated as weight solute/weight (solute + solvent) X 100. After preparation, samples were stored in sealed glass jars at 4°C in a commercial refrigerator. Portions (20 ml) of each sample were presented in 2-oz souffle cups labelled with randomized three-digit code numbers. Samples containing aspartame were prepared 1 h before testing to avoid the loss of sweetness that occurs during storage. All samples were removed from the refrigerator 1 h prior to testing and allowed to reach room temperature. Rating scales. Magnitude estimation scaling was used to evaluate perceived sweetness intensities of the samples (9). In this technique, samples are assigned a number proportional in intensity to a reference (modulus). A fixed modulus paradigm was used in which the modulus was assigned a value of 100. For example, if a sample tasted twice as sweet as the reference, it was assigned a value of 200; if it tasted half as sweet as the reference, it was assigned a value of 50. Pleasantness ratings were collected using a 15-cm visual analog scale, which was anchored at the left end with the phrase "extremely unpleasant" and at the right end with the phrase "extremely pleasant." Subjects were instructed to rinse with deionized water and wait 30 s between samples. All subjects expectorated the samples after tasting to avoid any glycemic effects of the sugars or psychodynamic stress to the diabetics associated with the consumption of sugar. Food records. Subjects kept daily food diaries for a period of 7 consecutive days. Subjects were trained by a nutritionist using
TEPPER, HARTFIEL AND SCHNEIDER
food models and familiar measuring tools to illustrate portion sizes. A standardized form was used to record all foods, condiments, and beverages consumed (except plain water), as well as the method of preparation, portion size, and time of consumption of each item. The completed food records were discussed with each subject to minimize erroneous reporting. Blood glucose measurements. Fasting blood samples were measured in a drop of blood obtained from the fingertip at the beginning of each of the three taste sessions. Glucose measurements were determined using the One Touch II blood glucose meter (Lifescan, Inc., Milpitas, CA).
Procedure Subjects participated in four 45-min morning sessions and were paid for each session completed. During the first session, subjects completed a screening questionnaire concerning their background, eating patterns, and smoking habits. A brief food frequency questionnaire composed of selected dietetic foods was incorporated into the larger questionnaire. Subjects also received instructions for keeping the 24-h food records. Lastly, subjects were trained in the use of magnitude estimation scaling by assigning magnitude estimates of sweetness intensity to the glucose solutions. Subjects reported to the remaining three sessions after an overnight fast, at which time a blood sample was taken for glucose determinations. During the second session, subjects assigned magnitude estimates of sweetness intensity to the beverage samples. The third session was a repeat of the second. Pleasantness ratings were assigned to the beverage samples at the final session. Sample presentation was randomized and all samples were evaluated in duplicate.
Data Analyses All magnitude estimates were converted to log values and plotted on log-log scales. Log magnitude estimates and pleasantness ratings were analyzed using repeated-measures analysis of variance (ANOVA) with diabetes classification and sweetener type as factors. The peak pleasantness rating was identified for each subject for all three sweeteners. Food records were coded and analyzed using the Nutritionist III Nutrient Data Base (Version 6.0, N2 Computing, Portland, OR), which is supplemented with information on selected carbohydrates (i.e., sucrose, fructose, lactose, and maltose) and contains a variety of commercially available sugar-free foods and beverages. Daily energy intakes and composition of the diet were calculated. Mean daily intakes of sucrose, fructose, aspartame, and saccharin were calculated. The analysis did not include other sugars (e.g., sorbitol) or alternative sweeteners because they were not regularly consumed by the subjects. It was also of interest to compare the amount of sweetness in the diabetic diet to that of the controls. To equate the sweetness derived from sugars to that derived from alternative sources, aspartame and saccharin intake was converted to gram amounts of sucrose equivalents. This conversion was based on the manufacturers' declaration that one packet of Equal (35 mg aspartame/packet) or Sweet'N Lo (Cumberland Packing Co., Brooklyn, NY; 40 mg saccharin/packet) provides the sweetening power of 12 g of sucrose. Dietary sweetness (i.e., grams of fructose + sucrose + alternative sucrose equivalents) was estimated from these calculations. The relationship between dietary sweetness estimates and peak pleasantness ratings for the test foods was evaluated using the pearson product moment correlation.
TASTE AND DIET IN DIABETES
15
TABLE 1 CHARACTERISTICSOF SUBJECTS
Lastly, the frequency of consumption of individual dietetic products was calculated from the food frequency questionnaire. These data were correlated with the responses tallied from the diet records as a check on the reliability of the latter instrument. Blood glucose measurements, age, body mass index (kg/m 2) and the various dietary measures were compared between subjects with diabetes and controls using the Student's t-test. Blood glucose measurements and incidence of neuropathies were correlated with hedonic and intensity ratings for the beverage samples to examine possible relationships between the measures of diabetic status and the taste ratings. All statistical analyses were conducted using the statistical package for the social sciences, SPSS/X. All values reported as significant had values of p _
Age (years) BMI ( k g / m 2) Fasting blood glucose ( m g / d l ) Glycosylated hemoglobin ( % ) t Duration of diabetes (years) Neuropathies (%) Diabetic treatment Diet alone (%) Insulin (%) Hypoglycemics (%) Other medications (%)
Subjects with Diabetes (n = 21)
Control Subjects (n = 16)
62.4 _+ 1.7 (range 4 3 - 7 2 ) 27.6 + 1.0 159.5 + 13.7" 8.6 + 2.8 8.3 ± 6.8 47.6
58.1 + 2.1 (range 4 4 - 7 3 ) 27.0 + 1.2 101.6 ± 2.7 ----
14.3 33.3 61.9 52.4
---43.8
RESULTS
Subject Characteristics Subject characteristics appear in Table 1. Subjects with diabetes and controls were well matched with respect to age and body mass index. Subjects with diabetes displayed mean fasting glucose and glycoslylated hemoglobin levels that were within acceptable limits of metabolic control (17). The majority of the subjects with diabetes were taking oral hypoglycemic agents and one-third received insulin treatment. Almost half of the subjects with diabetes had evidence of degenerative complications including cataract (14.2%), peripheral vascular disease (19%), and one or more types of peripheral neuropathies (38%; sensory and motor combined). Both subjects with diabetes and controls used various types of medications including diuretics and antihypertensive agents, vasodilators, and anticholesterolemics. Medication usage was of interest because many of these drugs are known to interfere with taste function (24).
Taste Ratings Perceived sweetness intensity of the beverage samples are shown in Fig. 1. In all subjects, perceived sweetness intensity of the samples increased with increasing sweetener concentration for all three sweeteners [ F ( 4 ) = 50.73, 76.84, and 42.43, p < 0.0001, for sucrose, fructose, and aspartame, respectively]. Subjects with diabetes tended to assign slightly higher intensity ratings to the samples with the lowest concentrations of sweeten-
Values are means ± SEM; values for men and women are combined. * Significantly different from controls at p < 0.0001. t Value is for 16 subjects for whom data were available; the upper limit o f normal is 5.8%.
ers than did controls, but this difference was not statistically reliable. Pleasantness ratings for the samples are shown in Fig. 2. Although pleasantness ratings increased with increasing sweetener concentration [ F ( 4 ) = 16.69, 29.54, 24.43, p < 0.001, for sucrose, fructose, and aspartame, respectively], no effect of diabetes on the pleasantness ratings was observed.
Relationships Between the Taste Ratings and Measures of Diabetic Status Magnitude estimates of sweetness intensity and perceived pleasantness ratings for the samples were not correlated with blood glucose measurements, evidence of neuropathies, or medication use in the subjects with diabetes. This was expected because no differences in intensity or pleasantness ratings were noted between subject groups.
Dietary Intake Measures of dietary intake are found in Table 2. Subjects with diabetes and controls consumed diets that were similar in energy content and composition. Estimates of dietary sweetness and the sources of this sweetness are graphically depicted in Fig. 3. The
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LOG % CONCENTRATION FIG. 1. Log mean magnitude estimates of sweetness intensity by subjects with diabetes (--) and controls (---) as a function of log % sweetener concentrationin Koolaid. No significantdifferencesbetween groups were found across concentrations.
16
TEPPER, HARTFIEL A N D SCHNEIDER
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FIG. 3. Mean estimated dietary sweetness content in the diabetic and control diet. Total dietary sweetness, defined as sucrose (solid bar)+ fructose (hatched bar)+ alternative sucrose equivalents (open bar), was similar in both groups. Subjects with diabetes consumed less sucrose ( p < 0.005) but more alternative sucrose equivalents ( p _<0.02) than did controls.
diabetic diet tended to be higher in sweetness than that of the controls, but this difference did not reach statistical significance. Although both groups consumed similar amounts of fructose, the subjects with diabetes consumed less sucrose than the controls ( p < 0.005). Sucrose comprised 5.4% of the carbohydrate energy in the diabetic diet compared to 19.7% of the carbohydrate energy in the control diet ( p < 0.01 by chi-square analysis). The majority of sweetness in the diabetic diet came from alternative sweeteners. Subjects with diabetes consumed an estimated 35 g of sucrose equivalents compared to an estimated 10 g of sucrose equivalents consumed by the controls ( p < 0.02). The relationship between dietary sweetness estimates and peak pleasantness ratings for the samples is illustrated in Fig. 4. Significant correlations were found for all three sweeteners in the subjects with diabetes ( r = +0.55, +0.49, and + 0 . 4 6 for sucrose, fructose, and aspartame, respectively; all p < 0.05) but not in the controls ( r = +0.35, +0.30, and + 0 . 2 4 ; NS).
Use of Low-Sugar Foods and Alternative Sweeteners The majority of the alternative sweeteners consumed by the subjects with diabetes was in the form of sweetener packets in coffee and tea and as diet soft drinks. Nonnutritive sweetener packets were used by 52% of the subjects with diabetes but only
TABLE 2 COMPOSITION OF THE DIET IN SUBJECTS WITH DIABETES AND CONTROLS Subjects
With
Diabetes
(n ~ 21)
Total energy (kcal/day) Protein (% of total energy) Fat (% of total energy) Carbohydrate (% of total enegy) Simple sugars (% of total energy) Complex carbohydrate (% of total energy) Alcohol (% of total energy) Values are means + SEM.
1965.9 + 94.1 19.4 + 0.5 32.0 + 1.7 48.3 + 1.8 15.1 + 1.1 33.7 + 1.8 0.3 -t- 0.1
Control
Subjects
(n = 16)
2173.6 + 137.6 16.9 + 0.6 32.6 + 1.5 48.3 + 1.9 16.6 + 1.0 30.8 + 1.8 2.5 ::t: 1.3
TASTE AND DIET IN DIABETES
__
17 DISCUSSION
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FIG. 4. Relationship between peak pleasantness ratings for the sweeteners in Koolaid and dietary sweetness content in subjects with diabetes (filled squares) and controls (open squares). Significant correlations were found for the subjects with diabetes only and are indicated by the solid lines. For the controls, r = +0.35, +0.30, and +0.24, NS, for sucrose, fructose, and aspartame, respectively.
26% of the controls ( p < 0.05 by chi-square analysis). Similarly, diet soft drinks were consumed by 65% of the subjects with diabetes as compared to only 25% of the controls ( p < 0.01 by chi-square analysis). Subjects with diabetes also consumed dietetic jams and jellies more often than controls ( p < 0.05). Dietetic product consumption tallied from the food records was highly correlated with food frequency questionnaire responses for foods that were regularly consumed. Significant correlations were found for sugar-free hot chocolate (r --- + 0.92, p < 0.01), diet soft drinks (r --- +0.86, p < 0.01), and dietetic jams and jellies (r = +0.40, p < 0.05).
Contrary to initial expectations, decreases in taste sensitivity to weak aqueous solutions that had previously been reported in diabetic populations (1,16,23,26) did not predict changes in the perception of sweetness in a real food. In the present study, subjects with type II diabetes and controls gave similar sweetness intensity ratings to a fruit beverage containing increasing concentrations of sucrose, fructose, or aspartame. The preference curves of the subjects with diabetes were also similar to those of controls, which is consistent with previous observations (8,16,22). Thus, when sweetness was incorporated into a real food, individuals with diabetes did not need more sweetening agent to attain the same sweetness level as controls. Taste deficits might have been more apparent among those who were poorly controlled (i.e., with higher fasting glucose values) or those with more severe neurological involvement (1,26). Interestingly, the subjects with diabetes gave slightly higher intensity ratings to the beverage samples at the lowest sweetener concentrations. This elevation in taste sensitivity at the lowest stimulus concentration is similar to that sometimes seen in the elderly (4). When only a weak stimulus was presented, elderly participants perceived a taste whereas younger subjects did not. This phenomenon has been attributed to the presence of a mild dysgeusia or background taste in the mouth (4). Abnormal dentition and poor oral health are thought to be the source of these disturbances. Because individuals with diabetes experience high rates of oral pathology, including periodontal disease, dental caries, recurrent infections, and burning mouth syndrome (11), dysguesias may be more prevalent among these individuals than in the general population. These subtle changes could distort the flavor of food and drink and need to be better documented in diabetic populations. Also, odor perception was not evaluated in this study and it is possible that differences in olfactory ability and hence flavor perception distinguish individuals with diabetes from those without the disease (26). In the present study, the subjects with diabetes consumed 32% of their energy as fat and 48% of their energy as carbohydrate. These values are consistent with current nutritional recommendations for people with diabetes mellitus (3). Other dietary surveys have reported that individuals with diabetes consumed 36-40% of total energy as fat and 41-43% of total energy as carbohydrate (12,20,21). Whether the dietary parameters found in our sample indicate better adherence to dietary goals or inaccuracy in dietary reporting is unknown. It was explained to the subjects in our study that their dietary adherence was not being evaluated. However, report bias, whether intentional or unintentional, cannot be ruled out (7). The analysis of dietary sweetness and source of the sweetness revealed important differences in the dietary habits of the subjects with diabetes compared to the controls. Subjects with diabetes consumed more alternative sweeteners and less sucrose than the controls. Alternative sweeteners were most frequently consumed in beverages including coffee, tea, and soft drinks. Diet soft drinks were well accepted among subjects with diabetes in our study, in agreement with previous work (13). The most novel finding of the current study was the observed relationship between the peak pleasantness ratings of the beverage samples and estimated dietary sweetness content of the diabetic diet. As a group, the subjects with diabetes did not consume more sweet foods than the controls. However, on an individual basis, those subjects with diabetes who habitually consumed more sweetness in their diets gave higher pleasantness ratings to the beverage samples. Thus, among individuals with diabetes who were well controlled, liking for the sweetened beverages appeared to be related to dietary intake than disrup-
18
TEPPER, HARTFIEL A N D SCHNEIDER
tions in sweet taste. These findings are generally consistent with other work examining the interaction of taste and nutrition such as salt taste in hypertension (20), and fat taste in dietary intake (19) and obesity (6,21). A greater understanding of this relationship in diabetes could lead to the design of better dietary manage-
ment strategies. Additional studies are needed to explore this possibility. ACKNOWLEDGEMENT We thank Marje Anderson of Robert Wood Johnson Hospital for her assistance in data collection.
REFERENCES 1. Abbasi, A. A. Diabetes: Diagnostic and therapeutic significance of taste impairment. Geriatrics 36:73-78; 1981. 2. American Dietetic Association. Position of the American Dietetic Association: Use of nutritive and nonnutritive sweeteners. J. Am. Diet. Assoc. 93:816-821; 1993. 3. American Diabetes Association. Nutritional recommendations and principles for people with diabetes mellitus: 1994. Diabetes Care 17:519-522; 1994. 4. Bartoshuk, L. M.; Rifkin, B.; Marks, L. E.; BARS, P. Taste and aging. J. Gerontol. 41:51-57; 1986. 5. Campbell, L. V.; Barth, R.; Gosper, J. Unsatisfactory nutritional parameters in noninsulin-dependent diabetes mellitus. Med. J. Aust. 151:146-150; 1989. 6. Drewnowski, A.; Kurth, C. L.; Rahaim, J. E. Taste preferences in human obesity: Environmental and familial factors. Am. J. Clin. Nutr. 54:635-641; 1991. 7. Dwyer, J. T.; Krall, E. A.; Coleman, K. A. The problem of memory in nutritional epidemiology research. J. Am. Diet. Assoc. 87:15091512; 1987. 8. Dye, C. J.; Koziatek, D. A. Age and diabetes effects on threshold and hedonic perception of sucrose solutions. J. Gerontol. 36:310-315; 1981. 9. Engen, T. Psychophysics. II. In: Kling, J. W.; Rigg, L. A., eds. Scaling methods in experimental psychology. 3rd ed. New York: Holt, 1971:47-86. 10. Fontvieille, A. M.; Faurion, A.; Heleal, I.; et al. Relative sweetness of fructose compared with sucrose in healthy and diabetic subjects. Diabetes Care 12:481-486; 1989. 11. Gibson, J.; Lamey, P-J.; Lewis, M. A. O.; Frier, B. M. Oral manifestations of previously undiagnosed noninsulin dependent diabetes mellitus. J. Oral Pathol. Med. 19:284-287; 1990. 12. Hess, D. A.; Setser, C. S. Comparison of aspartame- and fructosesweetened layer cakes: Importance of panels of users for evaluation of alternative sweeteners. J. Am. Diet. Assoc. 86:919-923; 1986. 13. Horwath, C. C.; Worsley. A. Dietary habits of elderly persons with diabetes. J. Am. Diet. Assoc. 91:553-557; 1991. 14. Kohn, H.; Goddard, K. A comparison of the American Diabetes Association 1984 diabetic dietary recommendations with the food intake of individuals with type I1 diabetes. Diabetes Educ. 11:25-29; 1985.
15. Laitinen, J. H.; Tuorila, H. M.; Uusitupa, M. I. J. Changes in hedonic responses to sweet and fat in recently diagnosed noninsulin-dependent diabetic patients during diet therapy. Eur. J. Clin. Nutr. 45:393400; 1991. 16. Lawson, W. B.; Zeidler, A.; Rubenstein, A. Taste detection and preference in diabetics and their relatives. Psychosom. Med. 41:219227; 1979. 17. Lebovitz, H. E. The physician's guide to noninsulin-dependent (type II) diabetes: Diagnosis and treatment. 2nd ed. Alexandria, VA: American Diabetes Association; 1988:25. 18. Le Floch, J-P.; Le Lievre, G.; Sadoun, J.; Perlemuter, L.; Peynegre, R.; Hazard, J. Taste impairement and related factors in Type I diabetes mellitus. Diabetes Care 12:173-178; 1989. 19. Mattes, R. D. Fat preference and adherence to a reduced-fat diet. Am. J. Clin. Nutr. 57:373-381; 1993. 20. Mattes, R. D.; Kumanyika, S. K.; Halpern, B. P. Salt taste responsiveness and preference among normotensive, prehypertensive and hypertensive adults. Chem. Senses 8:27-40; 1983. 21. Pangborn, R. M.; Bos, K. E. O.; Stern, J. S. Dietary fat intake and taste responses to fat in milk by under-, normal, and overweight women. Appetite 6:25-40; 1985. 22. Perlmuter, L. C.; Nathan, D. M.; Hakami, M. K.; Chauncy, H. H. Effect of noninsulin-dependent diabetes mellitus on gustation and olfaction. In: Kare, M. R.; Brand, J. G., eds. Interaction of the chemical senses with nutrition. New York: Academic Press; 1986:129-141. 23. Schelling, J. L.; Tetreault, L.; Lasagna, L.; Davis, M. Abnormal taste threshold in diabetes. Lancet 1:508-512; 1965. 24. Schiffman, S. S. Drugs influencing taste and smell perception. In: Getchell, T. V.; Doty, R. L.; Bartoshuk, L. M.; Snow, J. B., Jr., eds. Smell and taste in health and disease. New York: Raven Press; 1991:845-850. 25. Settle, R. G. Suprathreshold glucose and fructose sensitivity in individuals with different family histories of noninsulin-dependent diabetes mellitus. Chem. Senses 6:435-443; 1981. 26. Settle, R. G. The chemical senses in diabetes mellitus. In: Getchell, T. V.; Doty, R. L.; Bartoshuk, L. M.; Snow, J. B., Jr., eds. Smell and taste in health and disease. New York: Raven Press; 1991:829-844.
ELSEVIER
SSDI 0031-9384(95)02242-2
Sweet Taste and Diet in Type II Diabetes B E V E R L Y J. TEPPER, .1 L I S A M. H A R T F I E L * A N D STEPHEN H. S C H N E I D E R t
*Department of Food Science, Rutgers University, New Brunswick, NJ, and ?Department of Medicine, Division of Endocrinology, Metabolism and Nutrition, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson University Hospital, New Brunswick, NJ, USA Received 2 June 1995 TEPPER, B. J., L. M. HARTFIEL AND S. H. SCHNEIDER. Sweet taste and diet in type H diabetes. PHYSIOL BEHAV 60(1) 13-18, 1996.--The relationship between sweet taste function and dietary intake was studied in 21 patients with type II diabetes mellitus and 16 age-, weight-, and sex-matched controls. Subjects rated the sweetness intensity and pleasantness of a series of beverage samples sweetened with sucrose: 1.5-24%, fructose: 1-18%, or aspartame: 0.25-4%. They also kept 7-day food records. No group differences were found in sweet taste perception, pleasantness ratings, daily energy intakes, or macronutrient composition of the diets. However, subjects with diabetes consumed less sucrose but 3.5 times more alternative sweeteners than did controls. Peak pleasantness ratings for the beverage samples were positively correlated with dietary sweetness content in the subjects with diabetes but not the controls. These findings suggest that in diabetes, hedonic ratings for a sweetened beverage were related to dietary sweetness intake rather than changes in sweet taste perception. Diabetes
Taste
Sweetness
Diet
TYPE II (non-insulin-dependent) diabetes mellitus is characterized by abnormal carbohydrate metabolism and can be accompanied by a number of pathologic conditions affecting the kidney, eye, cardiovascular, and nervous systems. Diabetes also affects taste function, with sweet taste being the most vulnerable [see (26)]. Taste thresholds (e.g., the point at which a weak solution can be distinguished from plain water) are elevated in diabetic individuals for certain simple sugars including glucose (16,23) and sucrose (1,16). Although neurological complications appear to exacerbate taste deficits (1), they are not are critical for the expression of taste changes; taste deficits are also found in individuals with diabetes in the absence of neurological involvement (16) and in first-degree relatives who show no overt symptoms of the disease (16,25). A number of questions about the relationship between taste and diet in diabetes remain unanswered. First, with few exceptions (12,15) almost all studies examining taste in diabetes have used aqueous solutions rather than actual foods (1,8,10,16,22,23,25). Laboratory solutions lack the gustatory and textural qualities of complex foods and are often viewed as "test" solutions by subjects. Real foods need to be examined to determine whether such taste changes are nutritionally meaningful to individuals with diabetes. For example, if individuals with diabetes required more sweetening agent to attain the same level of sweetness in foods, then taste disturbances could make dietary
adherence difficult to achieve. Second, although a link between taste changes and dietary habits in diabetes has often been suggested, this relationship has never been directly tested. Studies are needed that examine both the taste and diet measures in the same individuals. Third, current recommendations support the utility of alternative sweeteners in the diabetic diet and such products are well accepted by the diabetic population (2,3). However, it is unclear whether individuals with diabetes experience changes in taste for these agents as they do for some of the simple sugars (12). The present study was undertaken to resolve these issues. The first objective was to evaluate sweet taste perception and pleasantness in a fruit beverage containing various levels of carbohydrate or alternative sweeteners in individuals with type II diabetes and control subjects. The second goal was to establish the dietary patterns of these individuals and evaluate possible relationships between the dietary factors and the taste ratings. METHOD
Subjects Subjects were 21 individuals with type II diabetes (15 men, 6 women) and 16 age- and weight-matched nondiabetic controls (10 men, 6 women). Individuals with diabetes were recruited by
1 Requests for reprints should be addressed to Beverly J. Tepper, Ph.D., Rutgers University, Department of Food Science, Cook College, P.O. Box 231, New Brunswick, NJ 08903.
13
14 their physicians at the Department of Endocrinology and Nutrition, Robert Wood Johnson University Hospital, and also by local newspaper advertisement. Control subjects were senior citizens recruited from local community centers and nontechnical employees of Rutgers University. Prior to acceptance into the study, all potential subjects were screened by telephone interview to ensure that they were in good health. Only those individuals with diabetes who exhibited good control (i.e., a recent fasting plasma glucose < 200 mg/dl), had been diagnosed at least 1 year prior to the study, and had normal kidney function were allowed to participate. Informed consent was provided by each subject on the first day of the study. In addition, medical histories were reviewed for the duration of diabetes, a recent glycosylated hemoglobin value (an indicator of long-term glycemic control), and current medication use. Evidence of degenerative complications was also recorded, including the incidence of cataract, peripheral vascular disease, and peripheral neuropathies (sensory and motor combined). All procedures were approved by the Institutional Review Boards of Rutgers University and the University of Medicine and Dentistry of New Jersey.
Experimental Measures Taste stimulus. The taste stimulus was a cherry-flavored beverage (Kraft General Foods, Inc., White Plains, NY; 2.1 g cherry Koolaid base/1 deionized water). Beverage samples were prepared with five concentrations of either sucrose (1.5%, 3%, 6%, 12%, and 24%), fructose (1%, 2%, 5%, 10.2%, and 18%), or the alternative sweetener aspartame (as Equal TM, G. D. Searle Co., Chicago, IL; 0.25%, 0.5%, 1%, 2%, and 4%.; Equal" provides 35 mg aspartame/packet). A pilot study revealed that the sweeteners were equisweet at the aforementioned concentrations. A series of glucose solutions was also evaluated as a training exercise to accustom the subjects to the use of the rating scales. Glucose solutions were prepared in five concentrations (3.1%, 7%, 10.5%, 19.8%, and 34.2%) in deionized water. All percentages were calculated as weight solute/weight (solute + solvent) X 100. After preparation, samples were stored in sealed glass jars at 4°C in a commercial refrigerator. Portions (20 ml) of each sample were presented in 2-oz souffle cups labelled with randomized three-digit code numbers. Samples containing aspartame were prepared 1 h before testing to avoid the loss of sweetness that occurs during storage. All samples were removed from the refrigerator 1 h prior to testing and allowed to reach room temperature. Rating scales. Magnitude estimation scaling was used to evaluate perceived sweetness intensities of the samples (9). In this technique, samples are assigned a number proportional in intensity to a reference (modulus). A fixed modulus paradigm was used in which the modulus was assigned a value of 100. For example, if a sample tasted twice as sweet as the reference, it was assigned a value of 200; if it tasted half as sweet as the reference, it was assigned a value of 50. Pleasantness ratings were collected using a 15-cm visual analog scale, which was anchored at the left end with the phrase "extremely unpleasant" and at the right end with the phrase "extremely pleasant." Subjects were instructed to rinse with deionized water and wait 30 s between samples. All subjects expectorated the samples after tasting to avoid any glycemic effects of the sugars or psychodynamic stress to the diabetics associated with the consumption of sugar. Food records. Subjects kept daily food diaries for a period of 7 consecutive days. Subjects were trained by a nutritionist using
TEPPER, HARTFIEL AND SCHNEIDER
food models and familiar measuring tools to illustrate portion sizes. A standardized form was used to record all foods, condiments, and beverages consumed (except plain water), as well as the method of preparation, portion size, and time of consumption of each item. The completed food records were discussed with each subject to minimize erroneous reporting. Blood glucose measurements. Fasting blood samples were measured in a drop of blood obtained from the fingertip at the beginning of each of the three taste sessions. Glucose measurements were determined using the One Touch II blood glucose meter (Lifescan, Inc., Milpitas, CA).
Procedure Subjects participated in four 45-min morning sessions and were paid for each session completed. During the first session, subjects completed a screening questionnaire concerning their background, eating patterns, and smoking habits. A brief food frequency questionnaire composed of selected dietetic foods was incorporated into the larger questionnaire. Subjects also received instructions for keeping the 24-h food records. Lastly, subjects were trained in the use of magnitude estimation scaling by assigning magnitude estimates of sweetness intensity to the glucose solutions. Subjects reported to the remaining three sessions after an overnight fast, at which time a blood sample was taken for glucose determinations. During the second session, subjects assigned magnitude estimates of sweetness intensity to the beverage samples. The third session was a repeat of the second. Pleasantness ratings were assigned to the beverage samples at the final session. Sample presentation was randomized and all samples were evaluated in duplicate.
Data Analyses All magnitude estimates were converted to log values and plotted on log-log scales. Log magnitude estimates and pleasantness ratings were analyzed using repeated-measures analysis of variance (ANOVA) with diabetes classification and sweetener type as factors. The peak pleasantness rating was identified for each subject for all three sweeteners. Food records were coded and analyzed using the Nutritionist III Nutrient Data Base (Version 6.0, N2 Computing, Portland, OR), which is supplemented with information on selected carbohydrates (i.e., sucrose, fructose, lactose, and maltose) and contains a variety of commercially available sugar-free foods and beverages. Daily energy intakes and composition of the diet were calculated. Mean daily intakes of sucrose, fructose, aspartame, and saccharin were calculated. The analysis did not include other sugars (e.g., sorbitol) or alternative sweeteners because they were not regularly consumed by the subjects. It was also of interest to compare the amount of sweetness in the diabetic diet to that of the controls. To equate the sweetness derived from sugars to that derived from alternative sources, aspartame and saccharin intake was converted to gram amounts of sucrose equivalents. This conversion was based on the manufacturers' declaration that one packet of Equal (35 mg aspartame/packet) or Sweet'N Lo (Cumberland Packing Co., Brooklyn, NY; 40 mg saccharin/packet) provides the sweetening power of 12 g of sucrose. Dietary sweetness (i.e., grams of fructose + sucrose + alternative sucrose equivalents) was estimated from these calculations. The relationship between dietary sweetness estimates and peak pleasantness ratings for the test foods was evaluated using the pearson product moment correlation.
TASTE AND DIET IN DIABETES
15
TABLE 1 CHARACTERISTICSOF SUBJECTS
Lastly, the frequency of consumption of individual dietetic products was calculated from the food frequency questionnaire. These data were correlated with the responses tallied from the diet records as a check on the reliability of the latter instrument. Blood glucose measurements, age, body mass index (kg/m 2) and the various dietary measures were compared between subjects with diabetes and controls using the Student's t-test. Blood glucose measurements and incidence of neuropathies were correlated with hedonic and intensity ratings for the beverage samples to examine possible relationships between the measures of diabetic status and the taste ratings. All statistical analyses were conducted using the statistical package for the social sciences, SPSS/X. All values reported as significant had values of p _
Age (years) BMI ( k g / m 2) Fasting blood glucose ( m g / d l ) Glycosylated hemoglobin ( % ) t Duration of diabetes (years) Neuropathies (%) Diabetic treatment Diet alone (%) Insulin (%) Hypoglycemics (%) Other medications (%)
Subjects with Diabetes (n = 21)
Control Subjects (n = 16)
62.4 _+ 1.7 (range 4 3 - 7 2 ) 27.6 + 1.0 159.5 + 13.7" 8.6 + 2.8 8.3 ± 6.8 47.6
58.1 + 2.1 (range 4 4 - 7 3 ) 27.0 + 1.2 101.6 ± 2.7 ----
14.3 33.3 61.9 52.4
---43.8
RESULTS
Subject Characteristics Subject characteristics appear in Table 1. Subjects with diabetes and controls were well matched with respect to age and body mass index. Subjects with diabetes displayed mean fasting glucose and glycoslylated hemoglobin levels that were within acceptable limits of metabolic control (17). The majority of the subjects with diabetes were taking oral hypoglycemic agents and one-third received insulin treatment. Almost half of the subjects with diabetes had evidence of degenerative complications including cataract (14.2%), peripheral vascular disease (19%), and one or more types of peripheral neuropathies (38%; sensory and motor combined). Both subjects with diabetes and controls used various types of medications including diuretics and antihypertensive agents, vasodilators, and anticholesterolemics. Medication usage was of interest because many of these drugs are known to interfere with taste function (24).
Taste Ratings Perceived sweetness intensity of the beverage samples are shown in Fig. 1. In all subjects, perceived sweetness intensity of the samples increased with increasing sweetener concentration for all three sweeteners [ F ( 4 ) = 50.73, 76.84, and 42.43, p < 0.0001, for sucrose, fructose, and aspartame, respectively]. Subjects with diabetes tended to assign slightly higher intensity ratings to the samples with the lowest concentrations of sweeten-
Values are means ± SEM; values for men and women are combined. * Significantly different from controls at p < 0.0001. t Value is for 16 subjects for whom data were available; the upper limit o f normal is 5.8%.
ers than did controls, but this difference was not statistically reliable. Pleasantness ratings for the samples are shown in Fig. 2. Although pleasantness ratings increased with increasing sweetener concentration [ F ( 4 ) = 16.69, 29.54, 24.43, p < 0.001, for sucrose, fructose, and aspartame, respectively], no effect of diabetes on the pleasantness ratings was observed.
Relationships Between the Taste Ratings and Measures of Diabetic Status Magnitude estimates of sweetness intensity and perceived pleasantness ratings for the samples were not correlated with blood glucose measurements, evidence of neuropathies, or medication use in the subjects with diabetes. This was expected because no differences in intensity or pleasantness ratings were noted between subject groups.
Dietary Intake Measures of dietary intake are found in Table 2. Subjects with diabetes and controls consumed diets that were similar in energy content and composition. Estimates of dietary sweetness and the sources of this sweetness are graphically depicted in Fig. 3. The
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16
TEPPER, HARTFIEL A N D SCHNEIDER
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FIG. 3. Mean estimated dietary sweetness content in the diabetic and control diet. Total dietary sweetness, defined as sucrose (solid bar)+ fructose (hatched bar)+ alternative sucrose equivalents (open bar), was similar in both groups. Subjects with diabetes consumed less sucrose ( p < 0.005) but more alternative sucrose equivalents ( p _<0.02) than did controls.
diabetic diet tended to be higher in sweetness than that of the controls, but this difference did not reach statistical significance. Although both groups consumed similar amounts of fructose, the subjects with diabetes consumed less sucrose than the controls ( p < 0.005). Sucrose comprised 5.4% of the carbohydrate energy in the diabetic diet compared to 19.7% of the carbohydrate energy in the control diet ( p < 0.01 by chi-square analysis). The majority of sweetness in the diabetic diet came from alternative sweeteners. Subjects with diabetes consumed an estimated 35 g of sucrose equivalents compared to an estimated 10 g of sucrose equivalents consumed by the controls ( p < 0.02). The relationship between dietary sweetness estimates and peak pleasantness ratings for the samples is illustrated in Fig. 4. Significant correlations were found for all three sweeteners in the subjects with diabetes ( r = +0.55, +0.49, and + 0 . 4 6 for sucrose, fructose, and aspartame, respectively; all p < 0.05) but not in the controls ( r = +0.35, +0.30, and + 0 . 2 4 ; NS).
Use of Low-Sugar Foods and Alternative Sweeteners The majority of the alternative sweeteners consumed by the subjects with diabetes was in the form of sweetener packets in coffee and tea and as diet soft drinks. Nonnutritive sweetener packets were used by 52% of the subjects with diabetes but only
TABLE 2 COMPOSITION OF THE DIET IN SUBJECTS WITH DIABETES AND CONTROLS Subjects
With
Diabetes
(n ~ 21)
Total energy (kcal/day) Protein (% of total energy) Fat (% of total energy) Carbohydrate (% of total enegy) Simple sugars (% of total energy) Complex carbohydrate (% of total energy) Alcohol (% of total energy) Values are means + SEM.
1965.9 + 94.1 19.4 + 0.5 32.0 + 1.7 48.3 + 1.8 15.1 + 1.1 33.7 + 1.8 0.3 -t- 0.1
Control
Subjects
(n = 16)
2173.6 + 137.6 16.9 + 0.6 32.6 + 1.5 48.3 + 1.9 16.6 + 1.0 30.8 + 1.8 2.5 ::t: 1.3
TASTE AND DIET IN DIABETES
__
17 DISCUSSION
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FIG. 4. Relationship between peak pleasantness ratings for the sweeteners in Koolaid and dietary sweetness content in subjects with diabetes (filled squares) and controls (open squares). Significant correlations were found for the subjects with diabetes only and are indicated by the solid lines. For the controls, r = +0.35, +0.30, and +0.24, NS, for sucrose, fructose, and aspartame, respectively.
26% of the controls ( p < 0.05 by chi-square analysis). Similarly, diet soft drinks were consumed by 65% of the subjects with diabetes as compared to only 25% of the controls ( p < 0.01 by chi-square analysis). Subjects with diabetes also consumed dietetic jams and jellies more often than controls ( p < 0.05). Dietetic product consumption tallied from the food records was highly correlated with food frequency questionnaire responses for foods that were regularly consumed. Significant correlations were found for sugar-free hot chocolate (r --- + 0.92, p < 0.01), diet soft drinks (r --- +0.86, p < 0.01), and dietetic jams and jellies (r = +0.40, p < 0.05).
Contrary to initial expectations, decreases in taste sensitivity to weak aqueous solutions that had previously been reported in diabetic populations (1,16,23,26) did not predict changes in the perception of sweetness in a real food. In the present study, subjects with type II diabetes and controls gave similar sweetness intensity ratings to a fruit beverage containing increasing concentrations of sucrose, fructose, or aspartame. The preference curves of the subjects with diabetes were also similar to those of controls, which is consistent with previous observations (8,16,22). Thus, when sweetness was incorporated into a real food, individuals with diabetes did not need more sweetening agent to attain the same sweetness level as controls. Taste deficits might have been more apparent among those who were poorly controlled (i.e., with higher fasting glucose values) or those with more severe neurological involvement (1,26). Interestingly, the subjects with diabetes gave slightly higher intensity ratings to the beverage samples at the lowest sweetener concentrations. This elevation in taste sensitivity at the lowest stimulus concentration is similar to that sometimes seen in the elderly (4). When only a weak stimulus was presented, elderly participants perceived a taste whereas younger subjects did not. This phenomenon has been attributed to the presence of a mild dysgeusia or background taste in the mouth (4). Abnormal dentition and poor oral health are thought to be the source of these disturbances. Because individuals with diabetes experience high rates of oral pathology, including periodontal disease, dental caries, recurrent infections, and burning mouth syndrome (11), dysguesias may be more prevalent among these individuals than in the general population. These subtle changes could distort the flavor of food and drink and need to be better documented in diabetic populations. Also, odor perception was not evaluated in this study and it is possible that differences in olfactory ability and hence flavor perception distinguish individuals with diabetes from those without the disease (26). In the present study, the subjects with diabetes consumed 32% of their energy as fat and 48% of their energy as carbohydrate. These values are consistent with current nutritional recommendations for people with diabetes mellitus (3). Other dietary surveys have reported that individuals with diabetes consumed 36-40% of total energy as fat and 41-43% of total energy as carbohydrate (12,20,21). Whether the dietary parameters found in our sample indicate better adherence to dietary goals or inaccuracy in dietary reporting is unknown. It was explained to the subjects in our study that their dietary adherence was not being evaluated. However, report bias, whether intentional or unintentional, cannot be ruled out (7). The analysis of dietary sweetness and source of the sweetness revealed important differences in the dietary habits of the subjects with diabetes compared to the controls. Subjects with diabetes consumed more alternative sweeteners and less sucrose than the controls. Alternative sweeteners were most frequently consumed in beverages including coffee, tea, and soft drinks. Diet soft drinks were well accepted among subjects with diabetes in our study, in agreement with previous work (13). The most novel finding of the current study was the observed relationship between the peak pleasantness ratings of the beverage samples and estimated dietary sweetness content of the diabetic diet. As a group, the subjects with diabetes did not consume more sweet foods than the controls. However, on an individual basis, those subjects with diabetes who habitually consumed more sweetness in their diets gave higher pleasantness ratings to the beverage samples. Thus, among individuals with diabetes who were well controlled, liking for the sweetened beverages appeared to be related to dietary intake than disrup-
18
TEPPER, HARTFIEL A N D SCHNEIDER
tions in sweet taste. These findings are generally consistent with other work examining the interaction of taste and nutrition such as salt taste in hypertension (20), and fat taste in dietary intake (19) and obesity (6,21). A greater understanding of this relationship in diabetes could lead to the design of better dietary manage-
ment strategies. Additional studies are needed to explore this possibility. ACKNOWLEDGEMENT We thank Marje Anderson of Robert Wood Johnson Hospital for her assistance in data collection.
REFERENCES 1. Abbasi, A. A. Diabetes: Diagnostic and therapeutic significance of taste impairment. Geriatrics 36:73-78; 1981. 2. American Dietetic Association. Position of the American Dietetic Association: Use of nutritive and nonnutritive sweeteners. J. Am. Diet. Assoc. 93:816-821; 1993. 3. American Diabetes Association. Nutritional recommendations and principles for people with diabetes mellitus: 1994. Diabetes Care 17:519-522; 1994. 4. Bartoshuk, L. M.; Rifkin, B.; Marks, L. E.; BARS, P. Taste and aging. J. Gerontol. 41:51-57; 1986. 5. Campbell, L. V.; Barth, R.; Gosper, J. Unsatisfactory nutritional parameters in noninsulin-dependent diabetes mellitus. Med. J. Aust. 151:146-150; 1989. 6. Drewnowski, A.; Kurth, C. L.; Rahaim, J. E. Taste preferences in human obesity: Environmental and familial factors. Am. J. Clin. Nutr. 54:635-641; 1991. 7. Dwyer, J. T.; Krall, E. A.; Coleman, K. A. The problem of memory in nutritional epidemiology research. J. Am. Diet. Assoc. 87:15091512; 1987. 8. Dye, C. J.; Koziatek, D. A. Age and diabetes effects on threshold and hedonic perception of sucrose solutions. J. Gerontol. 36:310-315; 1981. 9. Engen, T. Psychophysics. II. In: Kling, J. W.; Rigg, L. A., eds. Scaling methods in experimental psychology. 3rd ed. New York: Holt, 1971:47-86. 10. Fontvieille, A. M.; Faurion, A.; Heleal, I.; et al. Relative sweetness of fructose compared with sucrose in healthy and diabetic subjects. Diabetes Care 12:481-486; 1989. 11. Gibson, J.; Lamey, P-J.; Lewis, M. A. O.; Frier, B. M. Oral manifestations of previously undiagnosed noninsulin dependent diabetes mellitus. J. Oral Pathol. Med. 19:284-287; 1990. 12. Hess, D. A.; Setser, C. S. Comparison of aspartame- and fructosesweetened layer cakes: Importance of panels of users for evaluation of alternative sweeteners. J. Am. Diet. Assoc. 86:919-923; 1986. 13. Horwath, C. C.; Worsley. A. Dietary habits of elderly persons with diabetes. J. Am. Diet. Assoc. 91:553-557; 1991. 14. Kohn, H.; Goddard, K. A comparison of the American Diabetes Association 1984 diabetic dietary recommendations with the food intake of individuals with type I1 diabetes. Diabetes Educ. 11:25-29; 1985.
15. Laitinen, J. H.; Tuorila, H. M.; Uusitupa, M. I. J. Changes in hedonic responses to sweet and fat in recently diagnosed noninsulin-dependent diabetic patients during diet therapy. Eur. J. Clin. Nutr. 45:393400; 1991. 16. Lawson, W. B.; Zeidler, A.; Rubenstein, A. Taste detection and preference in diabetics and their relatives. Psychosom. Med. 41:219227; 1979. 17. Lebovitz, H. E. The physician's guide to noninsulin-dependent (type II) diabetes: Diagnosis and treatment. 2nd ed. Alexandria, VA: American Diabetes Association; 1988:25. 18. Le Floch, J-P.; Le Lievre, G.; Sadoun, J.; Perlemuter, L.; Peynegre, R.; Hazard, J. Taste impairement and related factors in Type I diabetes mellitus. Diabetes Care 12:173-178; 1989. 19. Mattes, R. D. Fat preference and adherence to a reduced-fat diet. Am. J. Clin. Nutr. 57:373-381; 1993. 20. Mattes, R. D.; Kumanyika, S. K.; Halpern, B. P. Salt taste responsiveness and preference among normotensive, prehypertensive and hypertensive adults. Chem. Senses 8:27-40; 1983. 21. Pangborn, R. M.; Bos, K. E. O.; Stern, J. S. Dietary fat intake and taste responses to fat in milk by under-, normal, and overweight women. Appetite 6:25-40; 1985. 22. Perlmuter, L. C.; Nathan, D. M.; Hakami, M. K.; Chauncy, H. H. Effect of noninsulin-dependent diabetes mellitus on gustation and olfaction. In: Kare, M. R.; Brand, J. G., eds. Interaction of the chemical senses with nutrition. New York: Academic Press; 1986:129-141. 23. Schelling, J. L.; Tetreault, L.; Lasagna, L.; Davis, M. Abnormal taste threshold in diabetes. Lancet 1:508-512; 1965. 24. Schiffman, S. S. Drugs influencing taste and smell perception. In: Getchell, T. V.; Doty, R. L.; Bartoshuk, L. M.; Snow, J. B., Jr., eds. Smell and taste in health and disease. New York: Raven Press; 1991:845-850. 25. Settle, R. G. Suprathreshold glucose and fructose sensitivity in individuals with different family histories of noninsulin-dependent diabetes mellitus. Chem. Senses 6:435-443; 1981. 26. Settle, R. G. The chemical senses in diabetes mellitus. In: Getchell, T. V.; Doty, R. L.; Bartoshuk, L. M.; Snow, J. B., Jr., eds. Smell and taste in health and disease. New York: Raven Press; 1991:829-844.