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Decreased sucrose preference in patients with type 2 diabetes mellitus
diabetes research and clinical practice 104 (2014) 214–219
Contents available at ScienceDirect
Diabetes Research and Clinical Practice jou rnal hom ep ag e: w ww.e l s e v i er . c om/ loca te / d i ab r es
Decreased sucrose preference in patients with type 2 diabetes mellitus Ji Hee Yu a, Mi-Seon Shin b,c, Jeong Rim Lee c,d, Jong Han Choi b,c, Eun Hee Koh b,c, Woo Je Lee b,c, Joong-Yeol Park b,c, Min-Seon Kim b,c,* a
Division of Endocrinology and Metabolism, Department of Internal Medicine, Korea University College of Medicine, Seoul, Republic of Korea b Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea c Diabetes Center, Asan Medical Center, Seoul, Republic of Korea d Outpatient Nursing Team, Asan Medical Center, Seoul, Republic of Korea
article info
abstract
Article history:
Aims: Increased sugar consumption may adversely affect glycemic control in patients with
Received 18 October 2013
diabetes. Although patients with diabetes are generally thought to prefer sweet tastes, few
Received in revised form
data are available on the sucrose preference in these individuals. The aim of the present
6 January 2014
study was to evaluate sucrose preference in patients with type 2 diabetes in comparison
Accepted 11 February 2014
with subjects without diabetes.
Available online 19 February 2014
Methods: Sucrose preference was assessed in 200 subjects (100 type 2 diabetes patients and 100 age-, sex- and body mass index (BMI)-matched control subjects). Sucrose preference was
Keywords:
evaluated together with sucrose perception (i.e., sucrose sensitivity). Clinical and biochem-
Sucrose
ical factors affecting sucrose taste were also analyzed.
Preference
Results: Participants with type 2 diabetes preferred lower sucrose concentrations compared
Sensitivity
with control subjects ( p = 0.001), although they had a less sensitive palate for sucrose
Diabetes
compared with subjects without diabetes ( p = 0.012). Individual sucrose preference demonstrated a negative relationship with sensitivity to sucrose in control subjects. Notably, this relationship between sucrose preference and sensitivity was completely absent in participants with type 2 diabetes. Male patients with diabetes demonstrated a higher sucrose preference compared with female patients. There were no significant correlations between sucrose preference and glycemic control, duration of diabetes, or anti-diabetic medications. Conclusions: Participants with type 2 diabetes demonstrate a lower preference for sweet tastes than control subjects despite their decreased perception of sucrose. Reduced sucrose preference is not associated with better glycemic control in individuals with diabetes. # 2014 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author at: Department of Internal Medicine, Asan Medical Center, Appetite Regulation Laboratory, Asan Institute for Life Sciences, University of Ulsan College of Medicine, 388-1 Poongnap-dong, Songpa-ku, Seoul 138-736, Republic of Korea. Tel.: +82 2 3010 3245; fax: +82 2 3010 6962. E-mail address: [email protected] (M.-S. Kim). http://dx.doi.org/10.1016/j.diabres.2014.02.007 0168-8227/# 2014 Elsevier Ireland Ltd. All rights reserved.
diabetes research and clinical practice 104 (2014) 214–219
1.
Introduction
Over the past few decades, the prevalence of type 2 diabetes mellitus (Type 2 DM) has dramatically increased across the globe [1]. Although Type 2 DM is a polygenic disorder, environment and behavioral factors contribute to the occurrence of Type 2 DM [2]. Epidemiological data have repeatedly demonstrated a strong positive association between the consumption of sugar-sweetened beverages and the development of Type 2 DM [3–5]. According to a recent meta-analysis, a single serving of a sugar-sweetened beverage per day increases the risk of diabetes by about 15% [6]. Furthermore, the increased consumptions of sucrose and sweetened foods by patients with diabetes potentially aggravate glycemic control. Thus, restricting sucrose intake might be of paramount importance in preventing and treating diabetes mellitus. An altered sensitivity for sweetness has been observed in patients with diabetes, and the ability to detect sweet tastes is impaired in type 1 and 2 diabetes [7–9]. Although previous studies report no changes in sucrose preference in small numbers of patients with diabetes [7,10], it is still uncertain whether a decreased sensitivity for sweetness in subjects with diabetes will enhance or decrease the preference for sugar in these individuals. Moreover, the precise factors that cause abnormally sweet tastes in patients with diabetes remain controversial [8,11–14]. In particular, the relationship between abnormal sweet taste and hyperglycemia in patients with diabetes still needs to be addressed [7,9,14]. Our present study was performed to evaluate sucrose preference in patients with Type 2 DM in conjunction with sucrose perception. We also sought to identify any clinical factors that affect sucrose taste in patients with diabetes.
2.
Subjects and methods
2.1.
Subjects
One hundred patients with Type 2 DM were recruited from a series of cases who attended the diabetes clinic at the Asan Medical Center (Seoul, Korea) between January and September 2012. Age-, sex-, and body mass index (BMI)matched healthy control subjects without diabetes (n = 100) were recruited from individuals visiting the health promotion center at the same hospital. The sample size was determined by the power calculation (b = 0.20, an error of a = 0.05) based on the result from a preliminary study. Individuals with type 1 diabetes, diabetes secondary to another disease, advanced renal disease, liver disease, active malignancy, another endocrine disease, psychiatric disorder(s), previous surgery (e.g., head and neck surgery, gastrointestinal surgery, transplantation), and certain previous or current medications (e.g., steroid hormones, thyroid hormones, sex hormones, antipsychotic agents) were excluded. All participants provided informed consent. The study protocol was approved by the institutional review board of Asan Medical Center.
2.2.
215
Procedures
All subjects underwent both sucrose preference and sensitivity tests in the morning following overnight fasting. Subjects were instructed to abstain from alcohol, tobacco, caffeine, and all beverages except water for 12 h before the tests. Sucrose sensitivity preceded sucrose preference testing, as the latter involved higher concentrations of sucrose solution. All solutions were prepared daily using distilled water and administered at room temperature. The following baseline clinical and biochemical characteristics were collected before testing: age, sex, BMI, systolic blood pressure (SBP), diastolic blood pressure (DBP), fasting plasma glucose (FBS), hemoglobin A1c (HbA1c), fasting total cholesterol, high-density lipoprotein (HDL)-cholesterol, low-density lipoprotein (LDL)cholesterol, triglycerides, smoking history, duration of diabetes, and any current anti-diabetic medications. Capillary blood glucose tests were also performed before testing. Tests were postponed for any patient whose glucose levels were below 3.9 mmol/L.
2.3.
Sucrose preference test
Sucrose preference was assessed using the forced-choice tracking technique [15]. This method has been proven to be useful for assessing preferences for sweets [16]. Subjects were presented with pairs of 2 different concentrations of sucrose solutions (5 mL each; 90, 180, 350, 700, and 1050 mM). For comparison, sodas such as Coca Cola (Atlanta, GA) are equivalent in sweetness to a 330 mM sucrose concentration. The first pair that was presented to each patient consisted of solutions from the middle range (180 mM and 700 mM). Subjects were asked to taste each without swallowing, then indicate which was preferred. The subsequent pair was determined by the subject’s prior preference choice. The procedure continued until the subject chose one concentration from pairs of both a higher and lower concentration or chose the highest or lowest sucrose solution two consecutive times. Subjects rinsed their mouth with water between each tasting. A one minute interval separated pairs of tastings. The entire task was repeated with stimulus pairs that were presented in reverse order. Sucrose preference was estimated from the mean sucrose concentrations of two trials.
2.4.
Sucrose sensitivity test
The two-alternative staircase method [17] was used to determine sucrose detection thresholds. For each trial, each subject was presented with pairs of solutions (5 mL sucrose solution and distilled water) and asked to determine which of the pair contained a taste. Subjects did not swallow the solutions and rinsed their mouth with distilled water prior to tasting each sample. 13 sucrose solutions ranging between 1 and 1000 mM were prepared by serial dilutions on a quarter log scale. The testing concentrations started at 3.2 mM. A single incorrect response resulted in a 1-step increase in the sucrose concentration at the beginning of the next trial, whereas two successive correct responses resulted in 1-step down. Reversal was defined as a change in the detectible sucrose concentration, either
216
diabetes research and clinical practice 104 (2014) 214–219
decreasing to increasing (negative reversal) or increasing to decreasing (positive reversal). The tests ended after 5 reversals. The sucrose detection threshold was calculated as the mean sucrose concentration of the last 4 reversals. Sucrose sensitivity is the inverse function of the sucrose detection threshold.
2.5.
Statistical analysis
Baseline characteristics between groups with or without diabetes were compared using the student t test for continuous data and the Chi-square test for categorical data. Pearson’s Chi-square test for linear trends was used to compare the proportions of subjects who chose each sucrose concentration on the sucrose preference and sensitivity tests. The relationship between sucrose preference and sensitivity was analyzed using the Spearman’s rank correlation coefficient. All statistical analyses were performed using SPSS (version 18.0; SPSS Inc., Chicago, IL). In this study, p < 0.05 is considered statistically significant.
3.
Results
3.1.
Subject characteristics
The clinical characteristics of the study subjects are listed in Table 1. The mean age of both study groups was 54 years (range, 30–70 years). Female subjects predominated in both groups. Compared with the control subjects, participants with Type 2 DM presented with higher plasma triglyceride and lower HDL-cholesterol levels, but lower LDL- and total cholesterol levels. The mean duration of diabetes was 10.3 years, and mean HbA1c was 8.4% (68 mmol/mol). Metformin, sulfonylurea, insulin, and insulin with oral hypoglycemic agents were taken by 78%, 60%, 40% and 31% of diabetic patients, respectively. Recent symptomatic hypoglycemic events within the previous week were observed in about 4% of subjects with diabetes.
3.2. DM
Decreased sucrose preference in patients with Type 2
Histograms of sucrose preference for the control group revealed a normal distribution pattern with a peak at the
Table 1 – Characteristics of the study subjects. Variable n Age (y) Sex Female (%) Male (%) BMI (kg/m2) Smoking Never (%) Former (%) Current (%) SBP (mmHg) DBP (mmHg) Total cholesterol (mg/dL) Triglyceride (mg/dL) HDL-cholesterol (mg/dL) LDL-cholesterol (mg/dL) FPG (mg/dL) HbA1c (%) HbA1c (mmol/mol)
Control
Type 2 DM
100 53.9 8.2
100 54.2 8.1
70 30 23.2 3.2
70 30 23.7 2.1
76 12 12 123.4 16.6 73.4 10.4 204.2 34.6 111.4 60.5 61.3 16.7 124.8 29.1 92.0 10.5 5.5 0.3 37.0 3.0
70 14 16 124.0 15.4 70.2 7.6a 167.0 32.3b 154.8 130.9b 53.4 16.9b 90.8 23.0b 155.9 49.1b 8.4 1.0b 68.0 11.0b
Data are the n (%) or the mean SD. BMI, body mass index; DBP, diastolic blood pressure; DM, diabetes mellitus; HDL, high-density lipoprotein; LDL, low-density lipoprotein; SBP, systolic blood pressure; FPG, fasting plasma glucose; HbA1c, hemoglobin A1c. a p < 0.05 vs. the control group. b p < 0.01 vs. the control group.
middle sucrose concentration (350 mM; Fig. 1A). In contrast, histograms of sucrose preference for the group with Type 2 DM were shifted to the left, i.e., toward a lower sucrose concentrations. Notably, 31% of the group with Type 2 DM chose the lowest sucrose concentration as the most preferred in comparison with only 12% of the control group ( p = 0.001; Fig. 1A). The ratio of Type 2 DM to the control subjects significantly decreased as the preferred sucrose concentration increased (Chi-square test for trend = 11.841; p = 0.001), indicating that individuals with diabetes preferred less sweet tastes compared with the control subjects. Histograms of the sucrose detection threshold for the control group were normally distributed (Fig. 1B). While the distribution of sucrose detection threshold for the group with Type 2 DM demonstrated a peak at the middle concentration (14 mM), it was skewed to the right (i.e., toward higher sucrose concentrations) compared with the control group (Chi-square test for trend = 6.357; p = 0.012). These data suggest that the
Fig. 1 – Distribution histograms of (a) sucrose preference and (b) sucrose detection thresholds in the control and Type 2 DM groups. Data are presented as the proportion of subjects (%).
diabetes research and clinical practice 104 (2014) 214–219
217
Fig. 2 – Relationship between sucrose preference and sensitivity in (a) the control and (b) Type 2 DM groups. Data are presented as the proportions of subjects (%). Rho indicates the Spearman’s correlation coefficient.
participants with Type 2 DM were less sensitive to the taste of sucrose compared with the control subjects.
and types of diabetic medication) demonstrated a significant association with sucrose sensitivity or preference.
3.3. Altered relationship between sucrose preference and sensitivity in patients with diabetes
4.
Individual sucrose sensitivity might affect sucrose preference and we thus plotted these factors together. Subjects were assigned to three groups based on the middle sucrose concentration determined using each test (low, normal, and high sucrose sensitivity groups [>, =, < 14 mM, respectively] and low, normal, and high sucrose preference groups [<, =, > 350 mM, respectively]). In the control group, sucrose sensitivity, which is inversely related to sucrose detection threshold, was found to negatively correlate with sucrose preference (rho = 0.292, p = 0.003; Fig. 2A), indicating that subjects with low sucrose sensitivity prefer sweeter tastes. However, this inverse relationship between sucrose preference and sensitivity was blunted in the group with Type 2 DM (rho = 0.187, p = 0.062; Fig. 2B). Indeed, a greater preference for the lowest sucrose concentration was observed in subjects with diabetes regardless of sucrose sensitivity (Fig. 2B).
3.4.
Factors related to sucrose taste
We analyzed the factors related to sucrose preference and sensitivity using Spearman’s correlation analysis. In the control group, male sex (rho = 0.240, p = 0.016) and smoking (rho = 0.244, p = 0.014) demonstrated a positive correlation with sucrose preference. On the other hand, the sucrose detection threshold was found to be positively associated with BMI (rho = 0.193, p = 0.049) and plasma triglycerides (rho = 0.254, p = 0.011), but negatively correlated with HDLcholesterol (rho = 0.256, p = 0.010). In the group with Type 2 DM, male sex was positively associated with sucrose preference (rho = 0.224, p = 0.027). No other factors (e.g., age, BMI, smoking, lipid profiles, hyperglycemia [FPG or HbA1c], duration of diabetes, recent hypoglycemic events within one week
Discussion
In our present study, we found that preferences for sweet taste were significantly lower among patients with Type 2 DM than age-, sex- and BMI-matched controls. A study performed in the 1970s reported that sucrose preference was not altered in a small number of patients with type 1 and 2 diabetes mellitus [7]. A recent study conducted on 25 women with gestational diabetes mellitus also reported no difference in the preference for sweet milk compared with women with normal pregnancies [18]. Our current data obtained from a large number of subjects with Type 2 DM are not in line with previous reports and go against the general belief that patients with diabetes might have a stronger preference for sweet tastes than healthy individuals without diabetes. Consistent with previous studies [7–9,11,12,14], the ability to detect sucrose was mildly impaired in our cohort of patients with diabetes. Abnormal sucrose perception in subjects with diabetes may lead to altered sucrose preference. In support of this possibility, we also found a good negative relationship between sucrose sensitivity and preference in our control subjects. That is, individuals who are more sensitive to sucrose have a weaker preference for sucrose. However, this inverse correlation between sucrose sensitivity and preference was found to be significantly blunted in our subjects with diabetes. Decreased sucrose preference was commonly found in subgroups of Type 2 DM patients with different sucrose sensitivities. Interestingly, this phenomenon was observed even in patients with Type 2 DM whose ability to detect sucrose was severely impaired. Although the reasons for the paradoxical decrease in sucrose preference we observed remain elusive, they may be related to hyperglycemia. In a previous study [19], sucrose preference was high in patients suffering from hypoglycemia. Consistently, streptozotocin-induced diabetic rats, which could have no conscious inhibition of sucrose intake, consume less sucrose
218
diabetes research and clinical practice 104 (2014) 214–219
solution than normal rats [20]. However, in our present Type 2 DM cohort, there was no significant association between sucrose preference and fasting glucose or glycated hemoglobin levels. Thus, hyperglycemia did not account for the decreased sucrose preference we observed in patients with diabetes. Other diabetes-associated factors, such as several complications of diabetes or anti-diabetic medications, may affect sucrose preference in patients with diabetes. In our present analysis, there was no significant association between individual sucrose preferences and their diabetes duration or current diabetic medications. These findings may lead us to speculate that a reduced sucrose preference might not be the result of diabetes-related biological changes and instead might reflect a psychological aversion to sweet foods. Patients with diabetes are aware that high sugar intake aggravates glycemic control, and this is probably reinforced through the educational materials provided by physicians and other medical staff members, books, internet, media, family, friends, etc. Indeed, it has frequently been reported that patients with Type 2 DM have increased dietary restraint [21,22], which may repress their desire for sweet foods and the pleasant feelings associated with these tastes. Analysis of the factors associated with sucrose taste reveal that male sex is positively associated with sucrose preference in subjects with or without diabetes, despite no sexual differences in sucrose sensitivity. Previous studies have shown that men prefer higher intensities of sweetness than women [23,24]. The reasons for these differences are currently unclear. Most likely, men might place fewer restrictions on sweet foods because they pay less attention to their body shapes and diets than women [25]. Meanwhile, we could not determine any diabetes-related factors that affect sucrose preference. In the subjects without diabetes, obesity, higher triglyceride levels, and lower HDLcholesterol levels were found to be significantly associated with a reduced sucrose sensitivity. These metabolic characteristics might be a consequence of the higher intake of sweet foods due to reduced sucrose sensitivity. In conclusion, our current data indicate that a sucrose preference is significantly lower in patients with Type 2 DM compared with age-, sex- and BMI-matched controls. Given that reduced sucrose preference was not associated with lower glycated hemoglobin levels, patients with diabetes might increase their intake of non-sweetened foods which were relatively free from the fear for sugar. Therefore, altered sucrose preferences in patients with diabetes should be considered when planning diets, education materials, and meals for these individuals.
Conflict of interest There are no conflict of interest.
Acknowledgement This study was supported by grants from the Asan Institute for Life Science (2013-0099) and the National Research Foundation of Korea Grant (2013M3C7A1056024), which is funded by the Korean government.
references
[1] Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence in adults for 2013 and projections for 2035 for the IDF diabetes atlas. Diabetes Res Clin Pract 2013. http:// dx.doi.org/10.1016/j.diabres.2013.11.002. [2] Kahm CR. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 1994;43:1066–85. [3] Malik VS, Popkin BM, Bray GA, Despres JP, Hu FB. Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk. Circulation 2010;121:1356–64. [4] Malik VS, Willett WC, Hu FB. Sugar-sweetened beverages and BMI in children and adolescents: reanalyses of a metaanalysis. Am J Clin Nutr 2009;89:438–9. author reply 439–40. [5] Vartanian LR, Schwartz MB, Brownell KD. Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis. Am J Public Health 2007;97:667–75. [6] Malik VS, Popkin BM, Bray GA, Despres JP, Willett WC, Hu FB. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care 2010;33:2477–83. [7] Lawson WB, Zeidler A, Rubenstein A. Taste detection and preferences in diabetics and their relatives. Psychosom Med 1979;41:219–27. [8] Le Floch JP, Le Lievre G, Sadoun J, Perlemuter L, Peynegre R, Hazard J. Taste impairment and related factors in type I diabetes mellitus. Diabetes Care 1989;12:173–8. [9] Perros P, MacFarlane TW, Counsell C, Frier BM. Altered taste sensation in newly-diagnosed NIDDM. Diabetes Care 1996;19:768–70. [10] Tepper BJ, Hartfiel LM, Schneider SH. Sweet taste and diet in type II diabetes. Physiol Behav 1996;60:13–8. [11] Chochinov RH, Ullyot GL, Moorhouse JA. Sensory perception thresholds in patients with juvenile diabetes and their close relatives. N Engl J Med 1972;286:1233–7. [12] Le Floch JP, Le Lievre G, Verroust J, Philippon C, Peynegre R, Perlemuter L. Factors related to the electric taste threshold in type 1 diabetic patients. Diabetic Med: J Br Diabetic Assoc 1990;7:526–31. [13] Abbasi AA. Diabetes: diagnostic and therapeutic significance of taste impairment. Geriatrics 1981;36:73–8. [14] Schelling JL, Tetreault L, Lasagna L, Davis M. Abnormal taste threshold in diabetes. Lancet 1965;1:508–12. [15] Mennella JA, Lukasewycz LD, Griffith JW, Beauchamp GK. Evaluation of the Monell forced-choice, paired-comparison tracking procedure for determining sweet taste preferences across the lifespan. Chem Senses 2011;36:345–55. [16] Asao K, Luo W, Herman WH. Reproducibility of the measurement of sweet taste preferences. Appetite 2012;59:927–32. [17] Wetherill GB, Levitt H. Sequential estimation of points on a psychometric function. Br J Math Stat Psychol 1965;18:1–10. [18] Tepper BJ, Seldner AC. Sweet taste and intake of sweet foods in normal pregnancy and pregnancy complicated by gestational diabetes mellitus. Am J Clin Nutr 1999;70: 277–84. [19] Mayer-Gross W, Walker JW. Taste and selection of food in hypoglycaemia. Br J Exp Pathol 1946;27:297–305. [20] Smith JC, Gannon KS. Ingestion patterns of food, water, saccharin and sucrose in streptozotocin-induced diabetic rats. Physiol Behav 1991;49:189–99. [21] Kenardy J, Mensch M, Bowen K, Pearson SA. A comparison of eating behaviors in newly diagnosed NIDDM patients and case-matched control subjects. Diabetes Care 1994;17:1197–9.
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[22] Mannucci E, Tesi F, Ricca V, Pierazzuoli E, Barciulli E, Moretti S, et al. Eating behavior in obese patients with and without type 2 diabetes mellitus. Int J Obes Relat Metab Disord: J Int Assoc Study Obes 2002;26:848–53. [23] Monneuse MO, Bellisle F, Louis-Sylvestre J. Impact of sex and age on sensory evaluation of sugar and fat in dairy products. Physiol Behav 1991;50:1111–7.
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Contents available at ScienceDirect
Diabetes Research and Clinical Practice jou rnal hom ep ag e: w ww.e l s e v i er . c om/ loca te / d i ab r es
Decreased sucrose preference in patients with type 2 diabetes mellitus Ji Hee Yu a, Mi-Seon Shin b,c, Jeong Rim Lee c,d, Jong Han Choi b,c, Eun Hee Koh b,c, Woo Je Lee b,c, Joong-Yeol Park b,c, Min-Seon Kim b,c,* a
Division of Endocrinology and Metabolism, Department of Internal Medicine, Korea University College of Medicine, Seoul, Republic of Korea b Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea c Diabetes Center, Asan Medical Center, Seoul, Republic of Korea d Outpatient Nursing Team, Asan Medical Center, Seoul, Republic of Korea
article info
abstract
Article history:
Aims: Increased sugar consumption may adversely affect glycemic control in patients with
Received 18 October 2013
diabetes. Although patients with diabetes are generally thought to prefer sweet tastes, few
Received in revised form
data are available on the sucrose preference in these individuals. The aim of the present
6 January 2014
study was to evaluate sucrose preference in patients with type 2 diabetes in comparison
Accepted 11 February 2014
with subjects without diabetes.
Available online 19 February 2014
Methods: Sucrose preference was assessed in 200 subjects (100 type 2 diabetes patients and 100 age-, sex- and body mass index (BMI)-matched control subjects). Sucrose preference was
Keywords:
evaluated together with sucrose perception (i.e., sucrose sensitivity). Clinical and biochem-
Sucrose
ical factors affecting sucrose taste were also analyzed.
Preference
Results: Participants with type 2 diabetes preferred lower sucrose concentrations compared
Sensitivity
with control subjects ( p = 0.001), although they had a less sensitive palate for sucrose
Diabetes
compared with subjects without diabetes ( p = 0.012). Individual sucrose preference demonstrated a negative relationship with sensitivity to sucrose in control subjects. Notably, this relationship between sucrose preference and sensitivity was completely absent in participants with type 2 diabetes. Male patients with diabetes demonstrated a higher sucrose preference compared with female patients. There were no significant correlations between sucrose preference and glycemic control, duration of diabetes, or anti-diabetic medications. Conclusions: Participants with type 2 diabetes demonstrate a lower preference for sweet tastes than control subjects despite their decreased perception of sucrose. Reduced sucrose preference is not associated with better glycemic control in individuals with diabetes. # 2014 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author at: Department of Internal Medicine, Asan Medical Center, Appetite Regulation Laboratory, Asan Institute for Life Sciences, University of Ulsan College of Medicine, 388-1 Poongnap-dong, Songpa-ku, Seoul 138-736, Republic of Korea. Tel.: +82 2 3010 3245; fax: +82 2 3010 6962. E-mail address: [email protected] (M.-S. Kim). http://dx.doi.org/10.1016/j.diabres.2014.02.007 0168-8227/# 2014 Elsevier Ireland Ltd. All rights reserved.
diabetes research and clinical practice 104 (2014) 214–219
1.
Introduction
Over the past few decades, the prevalence of type 2 diabetes mellitus (Type 2 DM) has dramatically increased across the globe [1]. Although Type 2 DM is a polygenic disorder, environment and behavioral factors contribute to the occurrence of Type 2 DM [2]. Epidemiological data have repeatedly demonstrated a strong positive association between the consumption of sugar-sweetened beverages and the development of Type 2 DM [3–5]. According to a recent meta-analysis, a single serving of a sugar-sweetened beverage per day increases the risk of diabetes by about 15% [6]. Furthermore, the increased consumptions of sucrose and sweetened foods by patients with diabetes potentially aggravate glycemic control. Thus, restricting sucrose intake might be of paramount importance in preventing and treating diabetes mellitus. An altered sensitivity for sweetness has been observed in patients with diabetes, and the ability to detect sweet tastes is impaired in type 1 and 2 diabetes [7–9]. Although previous studies report no changes in sucrose preference in small numbers of patients with diabetes [7,10], it is still uncertain whether a decreased sensitivity for sweetness in subjects with diabetes will enhance or decrease the preference for sugar in these individuals. Moreover, the precise factors that cause abnormally sweet tastes in patients with diabetes remain controversial [8,11–14]. In particular, the relationship between abnormal sweet taste and hyperglycemia in patients with diabetes still needs to be addressed [7,9,14]. Our present study was performed to evaluate sucrose preference in patients with Type 2 DM in conjunction with sucrose perception. We also sought to identify any clinical factors that affect sucrose taste in patients with diabetes.
2.
Subjects and methods
2.1.
Subjects
One hundred patients with Type 2 DM were recruited from a series of cases who attended the diabetes clinic at the Asan Medical Center (Seoul, Korea) between January and September 2012. Age-, sex-, and body mass index (BMI)matched healthy control subjects without diabetes (n = 100) were recruited from individuals visiting the health promotion center at the same hospital. The sample size was determined by the power calculation (b = 0.20, an error of a = 0.05) based on the result from a preliminary study. Individuals with type 1 diabetes, diabetes secondary to another disease, advanced renal disease, liver disease, active malignancy, another endocrine disease, psychiatric disorder(s), previous surgery (e.g., head and neck surgery, gastrointestinal surgery, transplantation), and certain previous or current medications (e.g., steroid hormones, thyroid hormones, sex hormones, antipsychotic agents) were excluded. All participants provided informed consent. The study protocol was approved by the institutional review board of Asan Medical Center.
2.2.
215
Procedures
All subjects underwent both sucrose preference and sensitivity tests in the morning following overnight fasting. Subjects were instructed to abstain from alcohol, tobacco, caffeine, and all beverages except water for 12 h before the tests. Sucrose sensitivity preceded sucrose preference testing, as the latter involved higher concentrations of sucrose solution. All solutions were prepared daily using distilled water and administered at room temperature. The following baseline clinical and biochemical characteristics were collected before testing: age, sex, BMI, systolic blood pressure (SBP), diastolic blood pressure (DBP), fasting plasma glucose (FBS), hemoglobin A1c (HbA1c), fasting total cholesterol, high-density lipoprotein (HDL)-cholesterol, low-density lipoprotein (LDL)cholesterol, triglycerides, smoking history, duration of diabetes, and any current anti-diabetic medications. Capillary blood glucose tests were also performed before testing. Tests were postponed for any patient whose glucose levels were below 3.9 mmol/L.
2.3.
Sucrose preference test
Sucrose preference was assessed using the forced-choice tracking technique [15]. This method has been proven to be useful for assessing preferences for sweets [16]. Subjects were presented with pairs of 2 different concentrations of sucrose solutions (5 mL each; 90, 180, 350, 700, and 1050 mM). For comparison, sodas such as Coca Cola (Atlanta, GA) are equivalent in sweetness to a 330 mM sucrose concentration. The first pair that was presented to each patient consisted of solutions from the middle range (180 mM and 700 mM). Subjects were asked to taste each without swallowing, then indicate which was preferred. The subsequent pair was determined by the subject’s prior preference choice. The procedure continued until the subject chose one concentration from pairs of both a higher and lower concentration or chose the highest or lowest sucrose solution two consecutive times. Subjects rinsed their mouth with water between each tasting. A one minute interval separated pairs of tastings. The entire task was repeated with stimulus pairs that were presented in reverse order. Sucrose preference was estimated from the mean sucrose concentrations of two trials.
2.4.
Sucrose sensitivity test
The two-alternative staircase method [17] was used to determine sucrose detection thresholds. For each trial, each subject was presented with pairs of solutions (5 mL sucrose solution and distilled water) and asked to determine which of the pair contained a taste. Subjects did not swallow the solutions and rinsed their mouth with distilled water prior to tasting each sample. 13 sucrose solutions ranging between 1 and 1000 mM were prepared by serial dilutions on a quarter log scale. The testing concentrations started at 3.2 mM. A single incorrect response resulted in a 1-step increase in the sucrose concentration at the beginning of the next trial, whereas two successive correct responses resulted in 1-step down. Reversal was defined as a change in the detectible sucrose concentration, either
216
diabetes research and clinical practice 104 (2014) 214–219
decreasing to increasing (negative reversal) or increasing to decreasing (positive reversal). The tests ended after 5 reversals. The sucrose detection threshold was calculated as the mean sucrose concentration of the last 4 reversals. Sucrose sensitivity is the inverse function of the sucrose detection threshold.
2.5.
Statistical analysis
Baseline characteristics between groups with or without diabetes were compared using the student t test for continuous data and the Chi-square test for categorical data. Pearson’s Chi-square test for linear trends was used to compare the proportions of subjects who chose each sucrose concentration on the sucrose preference and sensitivity tests. The relationship between sucrose preference and sensitivity was analyzed using the Spearman’s rank correlation coefficient. All statistical analyses were performed using SPSS (version 18.0; SPSS Inc., Chicago, IL). In this study, p < 0.05 is considered statistically significant.
3.
Results
3.1.
Subject characteristics
The clinical characteristics of the study subjects are listed in Table 1. The mean age of both study groups was 54 years (range, 30–70 years). Female subjects predominated in both groups. Compared with the control subjects, participants with Type 2 DM presented with higher plasma triglyceride and lower HDL-cholesterol levels, but lower LDL- and total cholesterol levels. The mean duration of diabetes was 10.3 years, and mean HbA1c was 8.4% (68 mmol/mol). Metformin, sulfonylurea, insulin, and insulin with oral hypoglycemic agents were taken by 78%, 60%, 40% and 31% of diabetic patients, respectively. Recent symptomatic hypoglycemic events within the previous week were observed in about 4% of subjects with diabetes.
3.2. DM
Decreased sucrose preference in patients with Type 2
Histograms of sucrose preference for the control group revealed a normal distribution pattern with a peak at the
Table 1 – Characteristics of the study subjects. Variable n Age (y) Sex Female (%) Male (%) BMI (kg/m2) Smoking Never (%) Former (%) Current (%) SBP (mmHg) DBP (mmHg) Total cholesterol (mg/dL) Triglyceride (mg/dL) HDL-cholesterol (mg/dL) LDL-cholesterol (mg/dL) FPG (mg/dL) HbA1c (%) HbA1c (mmol/mol)
Control
Type 2 DM
100 53.9 8.2
100 54.2 8.1
70 30 23.2 3.2
70 30 23.7 2.1
76 12 12 123.4 16.6 73.4 10.4 204.2 34.6 111.4 60.5 61.3 16.7 124.8 29.1 92.0 10.5 5.5 0.3 37.0 3.0
70 14 16 124.0 15.4 70.2 7.6a 167.0 32.3b 154.8 130.9b 53.4 16.9b 90.8 23.0b 155.9 49.1b 8.4 1.0b 68.0 11.0b
Data are the n (%) or the mean SD. BMI, body mass index; DBP, diastolic blood pressure; DM, diabetes mellitus; HDL, high-density lipoprotein; LDL, low-density lipoprotein; SBP, systolic blood pressure; FPG, fasting plasma glucose; HbA1c, hemoglobin A1c. a p < 0.05 vs. the control group. b p < 0.01 vs. the control group.
middle sucrose concentration (350 mM; Fig. 1A). In contrast, histograms of sucrose preference for the group with Type 2 DM were shifted to the left, i.e., toward a lower sucrose concentrations. Notably, 31% of the group with Type 2 DM chose the lowest sucrose concentration as the most preferred in comparison with only 12% of the control group ( p = 0.001; Fig. 1A). The ratio of Type 2 DM to the control subjects significantly decreased as the preferred sucrose concentration increased (Chi-square test for trend = 11.841; p = 0.001), indicating that individuals with diabetes preferred less sweet tastes compared with the control subjects. Histograms of the sucrose detection threshold for the control group were normally distributed (Fig. 1B). While the distribution of sucrose detection threshold for the group with Type 2 DM demonstrated a peak at the middle concentration (14 mM), it was skewed to the right (i.e., toward higher sucrose concentrations) compared with the control group (Chi-square test for trend = 6.357; p = 0.012). These data suggest that the
Fig. 1 – Distribution histograms of (a) sucrose preference and (b) sucrose detection thresholds in the control and Type 2 DM groups. Data are presented as the proportion of subjects (%).
diabetes research and clinical practice 104 (2014) 214–219
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Fig. 2 – Relationship between sucrose preference and sensitivity in (a) the control and (b) Type 2 DM groups. Data are presented as the proportions of subjects (%). Rho indicates the Spearman’s correlation coefficient.
participants with Type 2 DM were less sensitive to the taste of sucrose compared with the control subjects.
and types of diabetic medication) demonstrated a significant association with sucrose sensitivity or preference.
3.3. Altered relationship between sucrose preference and sensitivity in patients with diabetes
4.
Individual sucrose sensitivity might affect sucrose preference and we thus plotted these factors together. Subjects were assigned to three groups based on the middle sucrose concentration determined using each test (low, normal, and high sucrose sensitivity groups [>, =, < 14 mM, respectively] and low, normal, and high sucrose preference groups [<, =, > 350 mM, respectively]). In the control group, sucrose sensitivity, which is inversely related to sucrose detection threshold, was found to negatively correlate with sucrose preference (rho = 0.292, p = 0.003; Fig. 2A), indicating that subjects with low sucrose sensitivity prefer sweeter tastes. However, this inverse relationship between sucrose preference and sensitivity was blunted in the group with Type 2 DM (rho = 0.187, p = 0.062; Fig. 2B). Indeed, a greater preference for the lowest sucrose concentration was observed in subjects with diabetes regardless of sucrose sensitivity (Fig. 2B).
3.4.
Factors related to sucrose taste
We analyzed the factors related to sucrose preference and sensitivity using Spearman’s correlation analysis. In the control group, male sex (rho = 0.240, p = 0.016) and smoking (rho = 0.244, p = 0.014) demonstrated a positive correlation with sucrose preference. On the other hand, the sucrose detection threshold was found to be positively associated with BMI (rho = 0.193, p = 0.049) and plasma triglycerides (rho = 0.254, p = 0.011), but negatively correlated with HDLcholesterol (rho = 0.256, p = 0.010). In the group with Type 2 DM, male sex was positively associated with sucrose preference (rho = 0.224, p = 0.027). No other factors (e.g., age, BMI, smoking, lipid profiles, hyperglycemia [FPG or HbA1c], duration of diabetes, recent hypoglycemic events within one week
Discussion
In our present study, we found that preferences for sweet taste were significantly lower among patients with Type 2 DM than age-, sex- and BMI-matched controls. A study performed in the 1970s reported that sucrose preference was not altered in a small number of patients with type 1 and 2 diabetes mellitus [7]. A recent study conducted on 25 women with gestational diabetes mellitus also reported no difference in the preference for sweet milk compared with women with normal pregnancies [18]. Our current data obtained from a large number of subjects with Type 2 DM are not in line with previous reports and go against the general belief that patients with diabetes might have a stronger preference for sweet tastes than healthy individuals without diabetes. Consistent with previous studies [7–9,11,12,14], the ability to detect sucrose was mildly impaired in our cohort of patients with diabetes. Abnormal sucrose perception in subjects with diabetes may lead to altered sucrose preference. In support of this possibility, we also found a good negative relationship between sucrose sensitivity and preference in our control subjects. That is, individuals who are more sensitive to sucrose have a weaker preference for sucrose. However, this inverse correlation between sucrose sensitivity and preference was found to be significantly blunted in our subjects with diabetes. Decreased sucrose preference was commonly found in subgroups of Type 2 DM patients with different sucrose sensitivities. Interestingly, this phenomenon was observed even in patients with Type 2 DM whose ability to detect sucrose was severely impaired. Although the reasons for the paradoxical decrease in sucrose preference we observed remain elusive, they may be related to hyperglycemia. In a previous study [19], sucrose preference was high in patients suffering from hypoglycemia. Consistently, streptozotocin-induced diabetic rats, which could have no conscious inhibition of sucrose intake, consume less sucrose
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solution than normal rats [20]. However, in our present Type 2 DM cohort, there was no significant association between sucrose preference and fasting glucose or glycated hemoglobin levels. Thus, hyperglycemia did not account for the decreased sucrose preference we observed in patients with diabetes. Other diabetes-associated factors, such as several complications of diabetes or anti-diabetic medications, may affect sucrose preference in patients with diabetes. In our present analysis, there was no significant association between individual sucrose preferences and their diabetes duration or current diabetic medications. These findings may lead us to speculate that a reduced sucrose preference might not be the result of diabetes-related biological changes and instead might reflect a psychological aversion to sweet foods. Patients with diabetes are aware that high sugar intake aggravates glycemic control, and this is probably reinforced through the educational materials provided by physicians and other medical staff members, books, internet, media, family, friends, etc. Indeed, it has frequently been reported that patients with Type 2 DM have increased dietary restraint [21,22], which may repress their desire for sweet foods and the pleasant feelings associated with these tastes. Analysis of the factors associated with sucrose taste reveal that male sex is positively associated with sucrose preference in subjects with or without diabetes, despite no sexual differences in sucrose sensitivity. Previous studies have shown that men prefer higher intensities of sweetness than women [23,24]. The reasons for these differences are currently unclear. Most likely, men might place fewer restrictions on sweet foods because they pay less attention to their body shapes and diets than women [25]. Meanwhile, we could not determine any diabetes-related factors that affect sucrose preference. In the subjects without diabetes, obesity, higher triglyceride levels, and lower HDLcholesterol levels were found to be significantly associated with a reduced sucrose sensitivity. These metabolic characteristics might be a consequence of the higher intake of sweet foods due to reduced sucrose sensitivity. In conclusion, our current data indicate that a sucrose preference is significantly lower in patients with Type 2 DM compared with age-, sex- and BMI-matched controls. Given that reduced sucrose preference was not associated with lower glycated hemoglobin levels, patients with diabetes might increase their intake of non-sweetened foods which were relatively free from the fear for sugar. Therefore, altered sucrose preferences in patients with diabetes should be considered when planning diets, education materials, and meals for these individuals.
Conflict of interest There are no conflict of interest.
Acknowledgement This study was supported by grants from the Asan Institute for Life Science (2013-0099) and the National Research Foundation of Korea Grant (2013M3C7A1056024), which is funded by the Korean government.
references
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