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The Journal of Nutrition Vol. 128 No. 9 September 1998,
pp. 1481-1486
Research Department of Human Nutrition & Center of Food Research, The Royal Veterinary and Agricultural University, DK 1958 Frederiksberg, Denmark
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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In growth studies on rats, the ketohexose D-tagatose has been shown to contribute no net metabolizable energy, and a pronounced thermic effect of the sugar has been suggested to account for the absence of energy. In a double-blind and balanced cross-over design, we measured 24-h energy expenditure in eight normal weight humans in a respiration chamber during the consumption of 30 g D-tagatose or 30 g sucrose/d. Metabolic measurements were performed before and after a 2-wk adaptation period with a 30-g daily intake of the test sugar. Total 24-h energy expenditure and hour-by-hour profile were unaffected by the test sugar. The nonprotein respiratory exchange ratio (RERnp) was similar during consumption of D-tagatose and sucrose. However, the effect on RERnp due to CO2 produced by fermentation of D-tagatose could not be quantified in this study. A significant increase in 24-h H2 production (35%) during D-tagatose administration suggests a substantial malabsorption of the sugar. We found no effects of the 2-wk adaptation period on the measured gas exchange variables. Significantly lower fasting plasma insulin and triglyceride concentrations were observed during D-tagatose administration compared with the sucrose period. No effects of D-tagatose on body weight and composition were seen, but the perception of fullness 2.5 h after the sugar load was greater with D-tagatose. In conclusion, this study does not suggest a pronounced thermic effect of D-tagatose, and other mechanisms seem to be required to explain its lack of net energy.
KEY WORDS: D-tagatose · energy expenditure · fermentation · humans · hydrogen
Low energy bulk sweeteners are sugars or sugar alcohols that can be used as additives in the manufacture of low energy foods. Unlike intense sweeteners, low energy bulk sweeteners have a sweetening effect that is lower than or comparable to that of sucrose; thus, a greater volume of the sweetener is required. This is often useful in the manufacture of artificially sweetened food products. The low energy content of bulk sweeteners is often due to malabsorption, and daily consumption may therefore be limited by gastrointestinal side effects such as flatulence and diarrhea (Koutsou et al. 1996 When D-tagatose enters the liver, it is metabolized in much the same way as D-fructose. First, it is phosphorylated by ketohexokinase and then cleaved by aldolase B to enter glycolysis at the level of dihydroxy-acetone phosphate and D-glyceraldehyde (van den Berghe 1975 In this study, we investigated whether the intake of D-tagatose is associated with a marked thermogenesis both acutely and after a 14-d adaptation period, because exposure to nonabsorbed carbohydrates over a period of time may increase the fermentation capacity of the gut flora (Briet et al.(1995). Hydrogen and methane excretion were measured to detect any increase in fermentation when D-tagatose was administered. We took advantage of the study design to see whether the 15-d D-tagatose administration had an effect on liver function and blood lipids, which may be detectable in the fasting state.
Five Caucasian female subjects (weight 66.3 ± 2.9 kg, height 169.0 ± 2.3 cm, age 26.2 ± 2.63 y) and three Caucasian male subjects (weight 74.4 ± 3.9 kg, height 183.7 ± 0.8, age 25.0 ± 3.4 y), recruited through advertisements in local newspapers, took part in the study. Only nonsmokers were included in the study. Before inclusion, all candidates were screened for adverse responses (nausea or diarrhea) to D-tagatose. A single dose of 30 g of D-tagatose was administered at the screening. One candidate was excluded due to diarrhea; another subject was excluded because he felt uncomfortable with the indirect calorimetry procedure, although his symptoms probably did not relate to D-tagatose. The study protocol was approved by the Municipal Ethical Committee of Copenhagen and Frederiksberg, Denmark.
Statistics.
The effects of treatment and day on EE, RERnp and H2 production were tested by three-way ANOVA, with treatment, day and subject as categoric variables. Possible effects of treatment on the hour-by-hour profiles of RERnp were tested by the split-plot procedure. The effect of treatment on blood and urine parameters was tested for d 1, 7 and 15 separately by a paired t test and was also analyzed across the 3 d by the split-plot procedure. The analyses were performed with STATGRAPHICS version 4.2 (Graphic Software Systems, Rockville, MD) and SigmaStat 2.0 (Jandel Corporation, Erkrath, Germany). P-values < 0.05 were considered significant.
Body weight, fat-free mass, fat mass and blood pressure did not change significantly from d 1 to 15 (Table 1), and the across-period changes in weight and body composition were not found to be influenced by the nature of the test sugar (P > 0.25).
A pronounced thermogenic effect of D-tagatose has previously been proposed to explain the lack of net energy of the sugar when added to the basal diet seen in growth studies in rats (Levin et al. 1995
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). It has been suggested that D-tagatose, a stereoisomer of fructose, is absorbed to a greater extent than most other low energy bulk sweeteners, while still having a lower net energy content than sucrose (Levin et al. 1995). If this is true, then the gastrointestinal side effects of D-tagatose should be less because less of the sugar may be assumed to reach the large intestine, causing osmotic diarrhea and gas production from fermentation. The finding of a 68% recovery by breath of 14C from 14C-labeled D-tagatose given orally to adapted rats, (Levin et al. 1995) suggests that a substantial proportion of D-tagatose can be absorbed and metabolized in the body. However, the expiratory 14CO2 may, in fact, have derived from absorbed and subsequently metabolized fermentation products of D-tagatose (short-chain fatty acids, SCFA)5 or directly from bacterial degradation of D-tagatose. A recent study in pigs concluded that a maximum of 26% of ingested D-tagatose is absorbed at the level of the distal part of the small intestine (Johansen et al. 1997). This observation implies that the lack in net energy of D-tagatose reported from growth studies in rats (Levin et al. 1995, Livesey and Brown 1996) may be explained in part by malabsorption.
). Therefore D-tagatose probably has a metabolizable energy comparable to that of D-fructose. If most of it is absorbed, it should therefore be expected to have a strong thermic effect to account for its putative lack of net energy. A third possibility is that D-tagatose may impair the absorption of other macronutrients. This possibility has not as yet been examined.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). Fat-free mass was determined by measurements of weight, height and bioimpedance by using an algorithm presented by Heitmann (1990). The macronutrient composition of the diet was 50, 37 and 13 energy% carbohydrate, fat and protein, respectively. The controlled diet consisted of a continental breakfast (rye and wheat breads, butter, cheese, raspberry jam and orange juice), a lunch (rye and wheat breads, butter, salted ham, liver paste, cottage cheese with ham, cucumber, apple and fruit juice) and supper (goulash made with beef, onion, tomato purée, carrot, cream, cornflour, served with rice; and an apple).
). In addition to oxygen uptake and carbon dioxide production, we measured the production rates of hydrogen by nondispersive infrared absorption (URAS 3G, Hartmann & Braun AG, Frankfurt, Germany) and of methane by electrochemical sensor (STATOX-S, Computer Monitors Sensor Technology GmbH, Frankfurt, Germany). Total urine was collected for the following three periods: daytime (900-1830 h), post-supper (1830-2300 h) and night (2300-0900 h), and analyzed for total nitrogen excretion to calculate O2 and CO2 exchange not derived from protein oxidation. Protein oxidation was achieved by assuming that 6.25 g of protein was combusted per gram of nitrogen excreted in the urine (Brouwer 1965). Energy expenditure (EE) and nonprotein respiratory exchange ratio (RERnp) are presented as hour-by-hour profiles based on the assumption that nitrogen excretion was constant over each of the urine-sampling intervals. In four tests, hour-by-hour recordings of hydrogen production were lost due to a temporary sampling failure in the software. Data from the corresponding tests with the other test sugar were removed from the presentations and analyses. The calculation of EE does not take the formation of H2 and CH4 into account because the maximum recorded H2 and CH4 production within 1 h in any one experiment was 240 and 72 mL, respectively. Using the calculations of Poppitt et al. (1996), this corresponds to a reduction in EE of 1.15 and 0.19 kJ/h, respectively, or only ~0.3 and 0.05% of measured EE.
), insulin (RIA, Pharmacia and Upjohn, Copenhagen, Denmark), triglycerides (enzymatic test, Boehringer Mannheim Denmark, Ercopharm, Hørsholm), total cholesterol (HPTL chromatography, Boehringer Mannheim), HDL cholesterol (enzymatic test, Boehringer Mannheim; Sugiuchi et al. 1995) and urate (by microbial uricase and a peroxidase-catalyzed chromogenic process; Town et al. 1985). To test a possible effect of D-tagatose on liver function, we measured alkaline phosphatase (EC 3.1.3.1) (Boehringer Mannheim; Recommendations of the German Society for Clinical Chemistry 1970) and 
-glutamyl transferase (EC 2.3.2.2; Deutsches Arzneibuch der DDR 1968). In two subjects, serum was also analyzed for D-tagatose (capillary gas chromatography after deactivation of hydroxy groups; Jansen et al. 1986) to test whether the sugar remained detectable in blood 21 h after the load. Urine collections (24-h) from the metabolic study were analyzed for D-tagatose and urate to calculate their excretion rates. Additional analyses of fasting blood and 24-h urine collections from d 7 or 8 of the period were performed. The blood data for d 7 of one subject were excluded because she was not fasting when the samples were taken.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
Table 1.
Body weight and composition in eight fasting subjects in the morning after the first and last days of a 15-d period of consumption of 30 g D-tagatose or sucrose1,2
View larger version (16K):
[in a new window]
Fig 1.
Profiles of energy expenditure (EE) over a 24-h period in eight human subjects measured in a respiration chamber during consumption of 30 g D-tagatose or sucrose on the d 1 and 15 of an adaptation period with a daily intake of 30 g of the sugar.
View larger version (19K):
[in a new window]
Fig 2.
Profiles of nonprotein respiratory exchange ratio (RERnp) over a 24-h period in eight human subjects measured in a respiration chamber during consumption of 30 g D-tagatose or sucrose on d 1 and 15 of an adaptation period with a daily intake of 30 g of the sugar.
View this table:
Table 2.
Hydrogen production in subjects measured in a respiration chamber on the first and last days of a 15-d period of consumption of 30 g D-tagatose or sucrose1,2
View larger version (21K):
[in a new window]
Fig 3.
Profiles of hydrogen production in human subjects measured over a 24-h period in a respiration chamber during consumption of 30 g D-tagatose or sucrose on d 1 (n = 7) and d 15 (n = 5) of an adaptation period with a daily intake of 30 g of the sugar.
10 to 254 mL on d 1, and from 84 to 266 mL on d 15).
-glutamyl transferase, urate, blood lipids, glucose or insulin when D-tagatose was tested against sucrose separately for each of the three sampling occasions. However, when observations from the 3 d were merged into one analysis using a split-plot procedure, lower concentrations of insulin and triglycerides after D-tagatose were significant (insulin: D-tagatose vs. sucrose, d 1: 55.2 ± 4.0 vs. 64.4 ± 6.5; d 7: 59.3 ± 5.7 vs. 91.8 ± 20.8; d 15: 54.1 ± 3.9 vs. 58.2 ± 4.6 pmol/L, P = 0.05; triglycerides: D-tagatose vs. sucrose, d 1: 1.20 ± 0.13 vs. 1.38 ± 0.19; d 7: 1.37 ± 0.13 vs. 1.41 ± 0.17; d 15: 1.46 ± 0.22 vs. 1.70 ± 0.39 mmol/L, P = 0.04). Urinary urate excretion over a 24-h period from the chamber experiments tended to be increased by D-tagatose (D-tagatose vs. sucrose: 2.61 ± 0.18 vs. 2.29 ± 0.20 mmol, P = 0.09). No significant interactions between the nature of the sugar and point of time in the experimental period were found for urate excretion or any of the blood parameters. Of the four different perceived appetite scores, fullness 2.5 h after dinner was the only score that seemed to be affected by the nature of the test sugar, showing an increase with D-tagatose from 39 to 52% (P = 0.02). This response was similar on d 1 and 15.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, Livesey and Brown 1996). This was not confirmed by the present human study. In the rat studies, the daily load of D-tagatose was ~10% of gross energy, which is about twice the relative dose used in this study. Therefore it cannot be excluded that an increased energy expenditure compared with sucrose would have been disclosed with a higher load. However, the 30-g dose was chosen as a level that most humans could tolerate without unacceptable gastrointestinal symptoms. Furthermore, if the putative lack of net energy of D-tagatose were due solely to thermogenesis, an increase of ~5% in 24-h EE would be anticipated in this study. If most of this increase can be expected to occur within a few hours after the load, it should be above the detection limit based on calculations of within-subject variation of repeated measurements previously performed in our respiration chambers (Toubro et al. 1995). The 24-h indirect calorimetry tests were performed on d 1 of D-tagatose administration and after a 15-d period with regular intake to examine the possibility that an adaptation might increase the thermic effect of the sugar as a consequence of an improved recovery of its energy was examined. Repeated exposure of the colon to nonabsorbed carbohydrates may alter the intestinal flora and increase its capacity to ferment the carbohydrate (Briet et al. 1995), thus rendering a greater part of its energy available as absorptive SCFA. Moreover, studies with intravenous infusion of different SCFA suggest that they may be more thermogenic than glucose (Chioléro et al. 1993). In this study, total 24-h EE and hour-by-hour profiles of EE were very similar before and after the 2-wk intervention period, which does not indicate an increased energy expenditure as a consequence of adaptation (Fig. 1).
). The average increase of ~200 mL in the present study corresponds to 6.7 mL/g D-tagatose. This is between the values of 1.9 mL/g (obtained by ventilated hood; Bond and Levitt 1972) and 13.5 mL/g (obtained in a respiration chamber study; Christl et al. 1992) after ingestion of the nonabsorbable disaccharide lactulose. The higher values obtained from whole-body calorimetry studies may be due to the recovery of hydrogen in the flatus because <50% of H2 produced from rapidly fermented sugars may be excreted by the breath (Christl et al. 1992). Moreover, the amount of total hydrogen excretion is always subject to a pronounced interindividual variation which, in fact, makes it questionable to compare data concerning hydrogen production from different studies. The large between-subject variation in hydrogen release is probably due to ecological differences of the large intestine, resulting in different quantities of H2 being eliminated by the formation of different organic substances. The observation in this study that the only subject who produced appreciable amounts of methane had a low H2 excretion may reflect this mechanism. Comparing total 24-h H2 and CH4 production, or their hour-by-hour profiles over the days, did not give any indication that a possible change in fermentation capacity had occurred because no significant differences from d 1 to 15 were observed.
).
). However, an increase in H2 production of ~200 mL/d induced by D-tagatose is trivial compared with a daily O2 uptake of ~400 L. More unpredictable is the CO2 production associated with the formation of SCFA. An equation developed for the fermentation of hexoses in the colon of individuals with no methane production proposes that 1.68 mol CO2 is produced for each mole hexose degraded (Grimble et al. 1988). The fermentation of 25 g D-tagatose/d would add 5.2 L CO2 or ~1.5% to the measured CO2 production. In methane producers, CO2 is produced only in an amount that is equimolar to the degraded hexose (Miller and Wolin 1979). In addition to the CO2 produced by the fermentation, the various SCFA being formed are oxidized by the body at different RQ, e.g., the RQ of acetic acid and butyric acid are 1.00 and 0.80, respectively.
). Ritz et al. (1993) found 212 mL/g excessive CO2 on administration of 20 g lactulose. Both studies concluded that the observed increase in CO2 production would be sufficient to invalidate the calculation of substrate oxidations from respiratory gas exchange. The effect of CO2 produced by fermentation may be even greater in 24-h experiments using a respiration chamber compared with these short-term ventilated hood studies in which some of the CO2 produced may have accumulated in the colon or escaped the ventilated hood through flatus.
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FOOTNOTES |
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Manuscript received 22 January 1998. Initial reviews completed 6 March 1998. Revision accepted 21 May 1998.
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ACKNOWLEDGMENTS |
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We thank Charlotte Kostecki for the preparation of the experimental diet. We are also indebted to Anne Raben and Christina Cuthbertson of the Research Department of Human Nutrition, to Hans Bertelsen of MD Foods Ingredients, Denmark and to Albert Bär of Bioresco, Switzerland, who assisted with the preparation of the experimental protocol and manuscript.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results
Discussion
References
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-hydroxybutyrate on energy expenditure and substrate oxidation rates in lean humans.
Am. J. Clin. Nutr.
1993;
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