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Sweetener Augmentation of Serum Triacylglycerol during a Fat Challenge Test in Humans

Purdue University, Department of Foods and Nutrition (M.J.S., K.J., R.A.M.)
Indiana University Medical Center (C.H.)

Address reprint requests to: Richard Mattes, PhD, RD, Purdue University, Department of Foods and Nutrition, Stone Hall, Room 212, West Lafayette, IN 47907-1264

	ABSTRACT

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Objective: High concentrations of fructose enhance postprandial lipemia following lipid loading whereas glucose exerts a negative or minimal effect. This study evaluated the effect of lower sweetener concentrations and the contribution of their sweetness level and palatability.

Methods: At each of four test sessions, twelve male and ten female healthy adults ingested one of four milkshakes containing 108 g dairy cream alone or supplemented with 30 g fructose, 17.5 g glucose or 1 g aspartame. Blood samples were collected at baseline, two, four, six and eight hours after ingestion. Sensory discrimination tests were conducted after the last two sessions.

Results: Fructose and glucose led to 37% (p=0.03) and 59% (p=0.08) rises in triacylglycerol area under the curve (TG AUC) when compared to the plain milkshake, respectively. Although the sweetened shakes were equisweet and were more palatable than the plain shake, the TG rise after the aspartame milkshake did not differ from the plain milkshake.

Conclusions: These data indicate that low levels of glucose and fructose consumed with lipid enhance postprandial lipemia. Sweetness and palatability did not account for the effect.

Key words: triacylglycerol, human, glucose, fructose, taste

	INTRODUCTION

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The recommended initial approach for reducing coronary heart-disease risk is to improve lipid profiles by dietary means [1]. The postprandial period may be especially important [2,3]. Accumulating evidence indicates that ingestion of carbohydrate with lipid results in a prolonged elevation of plasma triacylglycerol (TG). Specifically, the addition of fructose or sucrose to an oral fat load elevates TG relative to a fat load without a sweetener [4–7]. In contrast, glucose has been reported to have a minimal or even a negative effect on the magnitude of postprandial triacylglycerolemia [5,8–10]. Consequently, it has been suggested that the augmentation is attributable to the fructose moiety [5,11].

A mechanism proposed to account for the contrasting effects between fructose and glucose holds that glucose elicits a larger release of insulin, which in turn stimulates lipoprotein lipase activity and TG clearance [12]. Fructose, on the other hand, evokes a smaller insulin and lipoprotein lipase response and is more readily taken up by the liver where it can promote endogenous TG synthesis. The elevated synthesis and reduced clearance of TG following fructose ingestion combine to augment postprandial lipemia. Consistent with this view, ingestion of a very high glucose load can completely suppress the postprandial rise of TG after a high fat meal [9] whereas lower glucose concentrations only diminish postprandial lipemia. However, these types of loading studies also suggest that at low concentrations, glucose may hold stimulating potential. When consumed at equal weights, the summated TG response to glucose is comparable to sucrose which comprises glucose and fructose [5]. This issue was explored in the present study with a lower concentration of glucose than has previously been tested.

This protocol also offered the opportunity to assess the effects of a more nutritionally representative exposure to fructose. The mean daily intake of fructose in the US diet is approximately 37 g/d [13]. Typical serving sizes of fruits, the most concentrated food sources, generally contribute less than 8 g and carbonated beverages, which supply about 39% of dietary fructose, contain about 15 g/12 oz [14]. Thus, ingestion of two sodas would provide about 30 g of fructose, the load used in the present study rather than 50 g as has often been administered.

Previously uncontrolled differences in the sensory properties (i.e., sweetness or palatability) of glucose and fructose could also account for their discrepant effects on the postprandial TG concentration. In rats, oral exposure to saccharin during gastric loading with lipid results in a prolonged TG elevation relative to the response following oral stimulation with water or no oral stimulation [15]. This suggests that sweetness alone may contribute to the TG response. Depending on the test method and concentration range, glucose is only 0.5 to 0.75 times as sweet as sucrose and fructose is 1.1 to 1.7 times sweeter than sucrose in aqueous solutions [16]. Sodium saccharin is 200 to 700 times as sweet as sucrose. Because glucose, sucrose and fructose were used on an equal-weight basis in previous studies [5–7], the weaker effect of glucose could be due to its lower sweetness. This issue was explored in the present study by contrasting TG responses to lipid loads made equisweet by the addition of fructose, glucose or aspartame.

The palatability of oral fat loads also could influence the postprandial response. Cohen et al. [17] reported an observation that ingestion of an unpalatable lipid load resulted in a delayed elevation of plasma TG relative to that noted with a more palatable stimulus. While no study has published data on the perceived pleasantness of the lipid loads used in fat-challenge studies, our pilot tests indicated that commonly used formulations [4–7] are unpleasant, in part because the high concentration of sweeteners used made them intensely sweet. The lipemic effect of sweeteners at lower, more palatable concentrations in lipid loads has not been explored, but could further augment their lipemic effects. While the concentrations of glucose used in the previous studies would likely have resulted in a less intensely sweet load, this is not the only sensory attribute influencing its palatability. Sugars have varying side flavors, different time courses of sensation impact and, as yet poorly characterized, interactions with other components in food systems that affect sensory properties. Glucose and fructose differ in a number of these dimensions [18], and this could account for the differential responses to these sweeteners. To explore this issue, responses to fat loads varying in palatability were contrasted.

	METHODS

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Subjects
Participants were recruited by public advertisement. They included 22 (twelve male, ten female) healthy adults, taking no medications and not adhering to any therapeutic diet. Their mean (±SD) age was 27.3±6.3 y and body mass index (BMI in kg/m²) was 25.3±4.5. Their customary fat intake, assessed by the Eating Pattern Assessment Tool (EPAT) [19], was 23.7±1.2 units on a scale ranging from 12 (low) to 40.

General Protocol
Participants were informed that the purpose of the study was to evaluate how the digestion of fat is influenced by the level of its intake. After a ten-hour overnight fast, a baseline blood sample (19 ml) was drawn from an antecubital vein. Subjects then consumed a milkshake in its entirety within one minute. This was followed by ingestion of 25 ml of water and the completion of chemosensory and health questionnaires. Subjects were allowed to leave the testing room between sessions, but returned to provide additional blood samples and complete health questionnaires at two, four, six and eight hours following ingestion of the lipid load. During this time, subjects continued to fast and refrained from both oral stimulation and strenuous exercise. Each participant completed four sessions during which milkshakes of varying composition were administered. Conditions were randomized and included 1) 108 g dairy cream, 2) 108 g dairy cream+30 g fructose, 3) 108 g dairy cream+17.5 g glucose, and 4) 108 g dairy cream+1 g aspartame. Because saccharin, the high intensity sweetener shown to enhance postprandial lipemia in rats [15], tasted bitter at the concentration needed to match the sweetness level of fructose, aspartame was used for this purpose. Glucose was used at a concentration judged as pleasant in pilot tests. At the end of the second session, participants were asked to complete the EPAT. Following both the third and fourth testing sessions, participants completed sensory tests in order to determine whether the milkshakes were distinguishable from one another. This protocol was approved by the Committee on the Use of Human Research Subjects at Purdue University. The test procedures were well tolerated except for slight and transient nausea reported by several subjects following milkshake ingestion. This nausea was not systematically related with any particular shake or time period.

Sensory Testing
A triangle test [20] was administered with the milkshake containing fructose and the milkshake containing aspartame following completion of the third treatment session. Ten sets of three stimuli (5 ml each) were presented, two alike and one different. Participants were required to sip and expectorate each stimulus and identify the odd sample. Participants rinsed with water between each sample. Testing was conducted under red light to mask subtle color differences between the samples. Room lighting was used during the experimental sessions because samples were never presented together. After the fourth treatment session, a modified Harris-Kalmus procedure [21] was conducted. Fourteen samples (5 ml each), seven containing fructose and seven containing aspartame, were presented in random order a single time and participants were asked to assign like samples to unique groups. Again, subjects rinsed with water between samples and red light was used to mask subtle color differences between the samples. Immediately following ingestion of each milkshake, participants rated them for sweetness, bitterness, saltiness, sourness, oiliness, creaminess, fat level and pleasantness on 15-point category scales with end anchors of "not at all" to "extremely" for intensity and "very unpleasant" and "very pleasant" for palatability.

Hematology
Plasma insulin and glucose concentrations were determined at baseline and two, four, six and eight hours after milkshake ingestion using a Linco Specific Human Insulin RIA Kit (St. Charles, MO) and a YSI Model 2300 Glucose analyzer, respectively. Serum TG, cholesterol and high density lipoprotein cholesterol (HDL) concentrations were also determined at these times by an enzymatic procedure using a Boehringer Manheim Hitachi 747 analyzer. Low-density lipoprotein cholesterol (LDL) concentration at each time point was calculated using the equation: LDL=(Cholesterol—HDL)—(TG/5).

Statistical Analysis
Due to a skewed distribution of data, the effects of different sweeteners, sweetness, and palatability on the primary dependent variable, plasma TG concentration, were assessed by Friedman Two-Way ANOVA. Wilcoxon Matched-Pairs Signed Ranks tests were conducted for paired comparisons where appropriate. Area under the curves (AUC) for TG, from stimulus ingestion to return to baseline, were computed by the trapezoidal method. Total, HDL and LDL cholesterol as well as insulin and glucose changes were analyzed by repeated-measures ANOVAs, since the distributions of these data were approximately normal. The within-subjects factors were form of stimulation (four levels) and time (five levels). Baseline measures of BMI, TG and insulin concentrations as well as EPAT results were correlated with peak and AUC TG values by Spearman’s Correlations. Gender effects were assessed by Friedman Two-Way ANOVA. Given the probabilities of random correct responses on the sensory tests, the criterion for assessing nonchance performance was correctly responding to 7 of 10 trials in the triangle test (p<0.05) and 12 of 14 samples for the Harris-Kalmus procedure (p<0.05). The criterion for statistical significance of all other tests was also set at p0.05. Analyses were conducted with release 6.12 of the SPSS for Windows statistical package (Chicago, IL) [22].

	RESULTS

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Table 1 contains TG values determined prior to milkshake ingestion on each treatment day (baseline) as well as values determined two, four, six and eight hours after consumption of each of the four challenges. Baseline TG concentrations were comparable prior to ingestion of each type of milkshake (²=3.9, df=3, p=0.27). Peak serum TG concentrations also did not differ significantly between conditions (²=5.9, df=3, p=0.12). AUC values differed significantly across treatments (²=8.4, df=3, p=0.04). The fructose supplemented milkshake resulted in a significantly higher value (38%) than the plain milkshake (z-score=2.1, p=0.03). Glucose supplementation resulted in a 60% higher AUC value than the plain milkshake, but due to higher variance associated with responses to glucose, this effect just failed to reach statistical significance (z-score=1.7, p=0.08). Both the fructose (z-score=2.0, p=.05) and glucose supplemented milkshakes (z-score=2.2, p=0.03) led to significantly higher AUC values compared to the aspartame treatment, 30% and 51%, respectively. There were no significant differences between responses to aspartame and plain (z-score=.26, p=0.79) or between fructose and glucose (z-score=0.63, p=0.53) sweetened shakes.

View larger version (30K): [in this window] [in a new window]   Fig. 1. Mean (SEM) change of serum triacylglycerol concentration from baseline after ingestion of milkshakes containing fructose, glucose, aspartame or no sweetener, (n=22). "*" signifies that all treatments significantly differ from baseline. "#" indicates that only the fructose and glucose conditions differ significantly from baseline.

Correlations between baseline TG concentration and peak TG value were significant in all four conditions (Table 2). Baseline TG concentration was also significantly correlated with TG AUC in the aspartame and glucose conditions. Baseline insulin concentration was not significantly associated with measures of TG AUC response, although it was significantly related with peak TG response in the plain, glucose, and fructose conditions and close to significant in the aspartame condition. Gender and EPAT scores were not significantly associated with TG peak or AUC treatment responses. Except with peak TG in the aspartame condition, BMI was not significantly associated with TG peak or AUC responses.

View larger version (23K): [in this window] [in a new window]   Fig. 2. Mean (SEM) sweet intensity (top panel) and pleasantness (bottom panel) of milkshakes containing fructose, glucose, aspartame or no sweetener, (n=22).

	DISCUSSION

The addition of fructose as sucrose yields variable results. A load of 50 g (100 g sucrose) led to a significantly greater postprandial peak TG concentration and summated response in one study [5], whereas supplementation with 57 g (114 g sucrose, mean of 1.5 g/kg dose) resulted in no significant change in either measure in another study [4]. However, in the latter work, the fructose treatment led to a significantly higher TG concentration six hours after dosing. No carbohydrate effect was reported with a 25 g (50 g sucrose) dose [5]. The less consistent TG responses to sucrose challenges may be attributable to the high concentration of glucose in the loads. The addition of 50 g glucose to an oral lipid load has led to a significant reduction in the summated postprandial TG concentration relative to an unsupplemented lipid load [5] and in doses ranging from 100–250 g, a rise of TG from baseline can be completely prevented [9]. In the present study, a dose of 17.5 g glucose elicited as large an elevation of summated TG and comparable peak values as the 30 g fructose load. Both led to greater summated TG responses than the unsupplemented load (albeit not quite significantly for glucose (p=0.08) and the proportions of participants showing the effect with the two sugars (70%) was comparable. Further TG concentration remained significantly above baseline six hours post-dosing with glucose and fructose, but not with the aspartame-sweetened or plain shakes.

While peak insulin levels may not have been captured due to the sampling scheme, at the time points measured, insulin concentrations were similar following glucose and fructose ingestion and neither led to a significant elevation relative to the lipid load alone. Insulin was not measured in previous studies, but, given the higher dose of glucose used and its potent effect on insulin release, it is likely plasma insulin levels were high in the studies reporting an inhibitory effect of glucose on fructose or sucrose augmentation of TG following lipid loading. The failure of glucose to suppress a TG response in the current study may be due to the weak effect the low-dose glucose stimulus had on insulin secretion. Insulin stimulates lipoprotein lipase (LPL) activity [23,24] and the carbohydrate-augmented postprandial rise of TG is due, at least in part, to decreased TG clearance [4]. It should be noted that this hypothesized mechanism may not hold under chronic feeding conditions where insulin stimulation of LPL activity may diminish [25,26].

Reduction of the potential insulin-mediated suppressive effect of glucose does not explain the higher TG concentration we observed with glucose supplementation of a lipid load. Enhanced endogenous TG synthesis and release alone or in combination with reduced clearance would be required to explain this phenomenon. Glucose could serve as a substrate for de novo TG synthesis, but ingestion of carbohydrate without lipid does not lead to an elevation of TG [4,27] and the observed marked rise in TG elicited by the low dose of glucose provided suggests this mechanism cannot fully account for the effect. This indicates that some other feature of nutritive sweeteners may promote the postprandial TG rise. A sensory contribution is suggested by the observation that hypertriacylglycerolemia is not observed with intravenous administration of a carbohydrate load that does lead to elevated TG following ingestion and stimulation of orosensory systems [28].

Sweetness is one feature examined in this study. Work in rats has demonstrated that oral stimulation with sodium saccharin accompanying the intragastric delivery of a lipid load results in a greater TG response than lipid loading alone [25]. The present data do not support such a role because the non-nutritive sweetener, aspartame, did not lead to an enhanced TG response relative to the unsweetened lipid load. Further, the response following aspartame was significantly lower than that observed after glucose or fructose supplementation when all three were judged as equisweet. However, a firm conclusion cannot be drawn because of the possibility that there are sweetener-specific effects. Differences in physiological responses to the sweetness of saccharin and aspartame have been observed. For example, aspartame is not an effective stimulus for cephalic phase insulin release in humans [29,30], whereas such a response has been noted with saccharin [31], although not consistently [29]. We did not use saccharin, an effective stimulus in rats, because, at the dose required to match sweetness levels with the nutritive sweeteners, the saccharin milkshakes were also distinctly bitter. A potential influence of cephalic-phase insulin release is supported by recent evidence that the early release of insulin is predictive of the postprandial concentration [32], which may, in turn, influence TG levels. In addition, at equal doses, a significantly greater suppression of TG is observed when glucose is administered orally with ingestion of a lipid load versus intravenously [5]. Ingestion of a nutritive sweetener alone (sucrose) does not elicit a rise of plasma triglycerides [4]. This indicates that either sweetness is not an effective stimulus in humans or that the mechanism involves an interaction between sensory quality and energy or lipid metabolism.

Oral stimulus palatability is another factor to consider. Cohen et al. [17] reported that ingestion of an unpalatable lipid load resulted in a delayed elevation of TG when compared to ingestion of a more palatable stimulus. In addition, more palatable stimuli have been found to elicit stronger pre-absorptive salivary, gastric and pancreatic responses that could influence digestion and absorption of lipid loads [33]. Pilot tests with previously used lipid-load formulations [4–7] revealed that these stimuli were unpleasant, partly because of excessive sweetness. In the present study, lower sweetener concentrations were used and pilot tests indicated that the glucose containing milkshake was more pleasant than the others. Study participants rated all three sweetened milkshakes as equally palatable and more pleasant than the unsweetened version. Consequently, the differential TG response observed between the nutritive and non-nutritive sweeteners fails to support an influence of palatability alone. However, while the sweetened milkshakes were more palatable than the unsweetened version, none were rated as actually pleasant. Thus, the stimuli may not have provided a full test of the palatability hypothesis.

In summary, the present data support previous findings that fructose augments postprandial lipemia following acute lipid loading in healthy adults [5–7], and that it does so at both the four-hour and the six-hour time points with nutritionally-relevant doses. In contrast to the view that glucose is an ineffective or inhibitory stimulus [5,10], the data show that, at a low dose, glucose is an effective stimulus for raising the postprandial TG concentration. Indeed, based on the fact that, at roughly half the concentration, it elicited a response comparable to fructose, it appears to hold potent stimulatory properties. Sensory testing failed to identify sweetness or palatability as explanations, but additional work will be needed to rule out these characteristics. Given the association between postprandial triacyglycerolemia and coronary heart disease risk [3], additional study of the factors that contribute to plasma TG concentrations are warranted. Low doses of oral glucose may be a useful tool in elucidating the mechanisms involved.

	ACKNOWLEDGMENTS

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The authors would like to thank Rebecca K. Mount and J. Antonio Sias for their assistance in the conduct of this study.

This work was supported by PHS grant #5 RO1 DK45294 from the National Institute of Diabetes and Digestive and Kidney Diseases and PHS MO1 RR00750.

Received May 1, 1998. Accepted December 1, 1998.

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This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Singleton, M. J. Articles by Mattes, R. D. Search for Related Content PubMed PubMed Citation Articles by Singleton, M. J. Articles by Mattes, R. D.