Sugar-sweetened-beverages (SSB) provide high amounts of rapidly absorbable sugar and have been shown to impair insulin sensitivity and promote weight gain. We hypothesized that when compared with high-glycemic index (GI) SSB low-GI SSB lead to lower insulin secretion and thus an improved preservation of insulin sensitivity and fat oxidation during an inactive phase.
In a controlled cross-over dietary intervention 13 healthy men (age: 23.7±2.2 years, body mass index: 23.6±1.9 kg m−2) consumed low-GI (isomaltulose) or high-GI (75% maltodextrin+25% sucrose, adapted for sweetness) SSBs providing 20% of energy requirement for 7 days. During this phase, participant's habitual high physical activity (11 375±3124 steps per day) was reduced (2363±900 steps per day). The provided ad libitum diet comprised 55% CHO, 30% fat and 15% protein. Glycemic and insulinemic responses were assessed: Day-long (7-day continuous interstitial glucose monitoring, 24-h-urinary c-peptide excretion), during meal test (37 g isomaltulose vs 28 g maltodextrin+9g sucrose) and measures of insulin sensitivity (basal: homeostasis model assessment of insulin resistance (HOMA-IR), postprandial: Matsuda-ISI). Macronutrient oxidation was assessed by non-protein respiratory quotient (npRQ) in the fasted state (npRQfasting) and postprandial as the area under the npRQ-curve during meal test (npRQtAUC-meal).
Day-long glycemia was lower with low-GI compared with high-GI SSB (−5%, P<0.05). Low-GI SSB led to lower insulin secretion during meal test (−28%, P<0.01) and throughout the day (−31%, P<0.01), whereas postprandial glucose levels did not differ between low-GI and high-GI SSBs. Insulin sensitivity deteriorated on inactivity with both SSBs, but was better preserved with low-GI isomaltulose compared with high-GI maltodextrin–sucrose (ΔHOMA-IR: +0.37±0.52 vs +0.85±0.86; ΔMatsuda-ISI: −5.1±5.5 vs −9.6±5.1, both P<0.05). Both, fasting and postprandial fat oxidation declined on inactivity, with no difference between high-GI and low-GI SSBs.
Compared with high-GI SSB, 7-day consumption of beverages sweetened with low-GI isomaltulose had beneficial effects on inactivity-induced impairment of glucose metabolism without effecting fuel selection.
Consumption of sugar-sweetened beverages (SSB) is very popular, especially among young men. In Europe the consumption of SSBs reaches up to 20% of energy intake.1, 2 Epidemiological and interventional studies indicate that a high intake of SSB is associated with the development of obesity3, 4 and type 2 diabetes.3, 5 Besides a high intake of liquid calories,4 SSBs provide large amounts of rapidly absorbable sugars, which lead to high glycemic and insulinemic responses.5 A continuous exposure to high levels of insulin has been shown to induce insulin resistance.6 In addition, insulin inhibits lipolysis and promotes fat storage.7, 8, 9 Ludwig10 therefore proposed that hyperinsulinemia associated with high-glycemic index (GI) diets may contribute to overweight. In line with this popular hypothesis, a diminished fat oxidation reflected by a high respiratory quotient (RQ), is considered as a metabolic predictor of weight gain independent of energy balance.11 Hence, a low fat oxidation in the fasted state (that is, a high RQfasting) is associated with higher prospective weight gain and fat storage11, 12 and a low postprandial fat oxidation (higher non-sleeping RQ, measured in a respiratory chamber) has been shown to impair weight maintenance after diet-induced weight loss.13
Even if a beneficial effect of a diminished insulin response with low-GI carbohydrates on fuel selection is plausible, robust scientific evidence is still lacking. Some studies showed an improved postprandial fat oxidation with low-GI carbohydrates14, 15, 16, 17 whereas others did not.18, 19, 20 Differences in food matrix, that is, solid or liquid form of test carbohydrates might contribute to equivocal results. Sugar in a liquid form has been shown to be worse for body weight regulation and glucose metabolism compared with sugar from solid sources.21, 22
Studies that investigated the effect of longer-term intake of low-GI carbohydrates on fasting macronutrient oxidation are rare and were conducted under metabolically challenging situations, for example, under excess carbohydrate and energy consumption20, 23 or during exercise.24 Physical inactivity also is a metabolically challenging condition that has been shown to diminish insulin sensitivity25 and fat oxidation.26 Thus physical inactivity might represent a phase that is vulnerable for adverse effects of SSB consumption.
Isomaltulose (Palatinose) is a slowly absorbable, low-GI (GI: 32, Atkinson et al.27) disaccharide that is used as an ingredient in sports drinks. Like sucrose, isomaltulose also consists of glucose and fructose and provides the same physiological energy.28 We hypothesize that beverages sweetened with low-GI isomaltulose compared with high-GI sucrose plus maltodextrin have a beneficial effect on maintenance of glucose metabolism and fuel selection. In a controlled cross-over dietary intervention, healthy men consumed either low-GI isomaltulose or high-GI (maltodextrin–sucrose) SSBs for 7 days while restricting physical activity below 3000 steps per day.
Subjects and methods
An outline of the study protocol is given in Figure 1. In a controlled cross-over dietary intervention, 16 healthy trained men (aged 19–26 years) consumed either low-GI (isomaltulose) or high-GI (75% maltodextrin+25% sucrose) sweetened beverages for 1 week (20% of daily energy requirement). Participant's habitual high physical activity was limited to <3000 steps per day. Macronutrient intake and physical activity were controlled during the study period. Wash out period between interventions was at least 3 weeks. Recruitment was done by advertisements on notice boards at the University Campuses in Stuttgart. Inclusion criteria were male sex and a habitual high physical activity level (exercise ⩾5 times per week and an active lifestyle with >10 000 steps per day). All participants were amateur athletes performing different types of endurance and strength trainings (for example, cycling, jogging, weight lifting exercises and team sports) but were no competitive sportsmen. The study population included male volunteers only because of hormonal perturbations during the female cycle. Volunteers with regular use of medication were excluded. One participant has been excluded because of weight loss efforts (−2.3 kg during 1 week) and two participants have been excluded because of significant differences in physical activity between low-GI and high-GI SSB intervention (2772 vs 11 417 steps per day; 2703 vs 6558 steps per day). The final study population comprised 13 men. The study protocol was approved by the ethics committee of the Medical council of Baden-Württemberg, Germany. All subjects provided written informed consent before participation.
Participants consumed 20% of their energy requirement in form of beverages sweetened with low-GI isomaltulose (Palatinose, Beneo GmbH, Mannheim, Germany) or high-GI maltodextrin (mixture of 75% maltodextrin6 (Nutricia GmbH, Erlangen, Germany) and 25% sucrose, adapted for sweetness). GI was 32 for isomaltulose and 90 for the mixture of maltodextrin and sucrose.27 Citric acid and non-nutritive flavoring agents were added to improve palatability. We conducted sensory tastings within the staff of our institute (n=12). Results revealed that a mixture of 75% maltodextrin and 25% sucrose had an equivalent sweetness when compared with isomaltulose. Individual energy requirements were calculated by multiplying resting energy expenditure (assessed by indirect calorimetry) by a sedentary physical activity level of 1.4 to estimate the amount of SSB provided during inactive phases. Participants were advised to consume the beverages in three portions in between meals. The total amount of low- or high-GI sugar consumed was 139±13 g per day. The beverages were provided in a single-blind randomized order. Three participants complained about gastrointestinal disturbances during the first 2 days while consuming isomaltulose. Dietary intake was ad libitum with a macronutrient composition of 55% carbohydrates, 30% fat and 15% protein. Dietary intake was controlled 3 days in advance of an active baseline measurement (to reach equal baseline conditions of macronutrient composition) and over the whole inactive intervention period. It has been shown that 3 days are sufficient to adapt macronutrient oxidation to energy and macronutrient content of a diet.29 All foods and beverages were provided and leftovers were back weighed to calculate accurate dietary intake (see Table 1). The provided diet had a GI of 53±8 and a glycemic load of 217±68 g per day (calculated according to WHO/FAO guidelines30 and based on information about GI of individual food items taken from the international tables of GI27).
Insulin sensitivity and insulin secretion
Interstitial glucose concentrations (CGM) were measured continuously by means of the Dexcom G4 glucose-monitoring device (Dexcom G4 Platinum, Nintamed GmbH & Co kg, Mainz, Germany) during both active baseline (7 day) and inactive (7 day) periods. The sensor was applied to the back of the upper arm to measure interstitial glucose concentration in the s.c. tissue. Sensor readings were reported every 5 min. The device was calibrated twice a day using capillary blood samples. Area under the glucose curve (AUC) was calculated as total AUC (tAUC) for the whole day (0900–2100 hours) using trapezoidal rule. Day-long insulin secretion was obtained by 24-h urinary c-peptide excretion at the end of activity and inactivity period using luminescence immunoassay method. Fasting blood samples were taken at the last 2 days of the active and inactive period after an overnight fast (>10 h). Fasting insulin and glucose values were averaged over these 2 consecutive days. Glucose was measured using hexokinase method and serum insulin was determined by electrochemiluminescence. Fasting insulin sensitivity was obtained by homeostasis model assessment of insulin resistance (HOMA-IR): fasting glucose (mmol l−1) × fasting insulin (mU l−1)/22.5.31 A standard 75-g oral glucose tolerance test (OGTT) was performed at active baseline and at the end of intervention, with blood sampling for glucose and insulin analysis at 0, 30, 60, 90, 120 and 180 min. Postprandial insulin sensitivity was calculated by Matsuda whole-body insulin sensitivity index (Matsuda-ISI): 10 000/(√(fasting glucose × fasting insulin) × (mean glucose × mean insulin during OGTT)).32 Postprandial glucose and insulin responses to low-GI isomaltulose and high-GI SSB were tested as tAUC during a meal test at the end of the active and inactive periods (37 g isomaltulose vs 28 g maltodextrin+9 g sucrose).
and were continuously measured by open circuit indirect calorimetry in the morning after an overnight fast (ventilated hood system, Quark RMR, Cosmed, Rome, Italy). Measurements were performed for ⩾30 min and only steady-state periods were used for calculations. The non-protein RQ (npRQ; RQ corrected for nitrogen excretion) and the amount of carbohydrate, protein and fat oxidation were calculated according to the study by Jéquier et al.33 N-excretion in 24-h urine was calculated from photometric measured urea concentration and obligate N-losses by feces and skin were assumed as +2.5 g N. npRQfasting was averaged from two single measurements on consecutive days. Postprandial fuel selection was calculated as total area under the npRQ-curve (npRQtAUC-meal) during the meal test. Measurements were performed at baseline (npRQ fasting), 30–60, 90–120 and 150–180 min after SSB intake.
Body composition and physical activity
Height was measured using a stadiometer (seca 274, seca GmbH&Co.KG, Hamburg, Germany). Body weight and fat mass were measured on a calibrated impedance scale (seca mBCA 515, seca GmbH&Co.KG). Participants were requested to abstain from exercise and to reduce their everyday activity to <3000 steps per day during the intervention periods to control for physical activity and to induce a vulnerable metabolic situation. Participants were also instructed to refrain from rigorous exercise 1 day prior to active baseline measurements. Physical activity was continuously measured using a triaxial activity monitor (ActivPAL, Paltechnologies Ltd., Glasgow, UK). The ActivPAL device was continuously worn on the upper thigh fixed with a waterproof patch.
Data are expressed as means±s.d. Normal distribution was checked by Kolmogorov–Smirnov test. A priori power analysis revealed that 12 individuals were required to detect a 15% difference in insulin sensitivity assuming a statistical power of 80% and a 5% significance level. Differences between low-GI isomaltulose and high-GI maltodextrin+sucrose were tested by two-tailed paired t-test. Differences in active baseline values were considered as a covariate using repeated measures analysis of covariance. Differences in the composition of dietary intake were analyzed using repeated measures analysis of variance. Analyses were conducted using SPSS statistical software (SPSS 22.0, IBM Corporation, Armonk, NY, USA). Two-tailed P-values<0.05 were considered to indicate statistical significance.
Dietary intake is shown in Table 1. Macronutrient intake at single days ranged between 47 and 61% CHO, 23 and 38% fat and 11 and 20% protein. Compared with the physical active phase, participants consumed more carbohydrates and less protein during inactivity with both SSB interventions (CHO:+3–5% energy, protein: −3% energy, all <0.05). In addition, with the high-GI SSB consumption energy and fat intake were slightly lower during inactivity compared with activity (energy: −6%; fat: −3% energy, all P<0.05). Energy and macronutrient intake during inactive periods did not differ between low-GI isomaltulose and high-GI maltodextrin+sucrose.
Baseline anthropometric data and physical activity are indicated in Table 2. Participants were aged 19–26 years and had a body mass index between 20.8 to 28.0 kg m−2 and a percent body fat (%FM) between 6.0 and 25.4%. A slight weight loss was observed with high-GI SSB consumption (P<0.05). Fat mass significantly increased with inactivity in both SSB interventions (both, P<0.05). Changes in body weight and body composition did not differ between high-GI and low-GI interventions. Mean reduction in physical activity was approximately −80%. There was no difference in physical activity between low-GI and high-GI SSB intervention periods. Also the changes in physical activity due to activity restriction did not differ.
Changes in glucose metabolism due to inactivity and SSB intervention are shown in Table 3. Compared with active baseline measurements, day-long glycemic and insulinemic responses were higher during the inactive intervention period with high-GI maltodextrin+sucrose, but not with low-GI isomaltulose (Table 3). During inactivity, participants had a −5% lower day-long glycemic response (P<0.05) and a −31% lower 24-h c-peptide excretion (P<0.01) with low-GI isomaltulose compared with high-GI maltodextrin+sucrose (Figure 2). Fasting insulin increased with the high-GI SSB on inactivity, but remained unchanged with the low-GI SSB. At the end of the low-GI intervention, levels of fasting insulin were −16% lower compared with the respective high-GI period (P<0.05). There was no effect of inactivity or SSB intervention on fasting blood glucose (Table 3). Fasting and postprandial insulin sensitivity decreased with inactivity in both SSB interventions, but the decline was less with low-GI isomaltulose compared with high-GI maltodextrin+sucrose (Table 3). Before the high-GI intervention participants had a slightly higher baseline insulin sensitivity (Matsuda-ISI P<0.05), but the GI effect remained significant after controlling for these differences (repeated measures analysis of covariance, P<0.05). Glycemic and insulinemic responses during meal tests are indicated in Figure 3. Compared with high-GI SSB, low-GI isomaltulose led to a lower postprandial insulin secretion during the meal test, both within active and inactive conditions (−27% at the end of activity, P<0.001; −28% at the end of inactivity, P<0.01). These results remained significant when comparing iAUC instead of tAUC values. Glycemic response during the meal test was prolonged with low-GI sugar under active conditions, whereas no difference in glycemic response between low-GI and high-GI SSB was observed during inactive conditions. There was no difference in glucagon response between low-GI and high-GI meal tests during inactivity (glucagontAUC: 470±187 vs 449±243 ng l−1 per 3h; P>0.05).
Changes in fuel selection on inactivity are compared between the low-GI and high-GI intervention in Table 3. npRQfasting increased equally due to inactivity with high-GI and low-GI SSB. Postprandial fuel selection (npRQtAUC-meal) showed a lower increase due to inactivity with low-GI compared with high-GI SSB (Table 3). Carbohydrate oxidation was higher at the expense of fat oxidation with low-GI isomaltulose than with high-GI maltodextrin+sucrose (Figure 3) during active conditions. After 1 week of physical inactivity, postprandial substrate use did not differ between high-GI and low-GI meal tests.
We hypothesized that when compared with high-GI SSB, low-GI SSB lead to lower insulin secretion and thus an improved preservation of insulin sensitivity and fat oxidation during an inactive phase. In line with this hypothesis, insulin secretion was lower and insulin sensitivity was higher after 1-week consumption of beverages sweetened with low-GI isomaltulose compared with high-GI maltodextrin plus sucrose. The difference in insulin secretion had, however, no effect on fasting and postprandial fuel selection.
Impact of low- vs high-GI SSB on glucose metabolism
The present study has shown that when compared with high-GI SSB, beverages sweetened with low-GI isomaltulose led to lower insulin responses during the meal test (Figure 3) and less cumulative insulin secretion throughout the day (Figure 2). Contrary to the GI-concept, postprandial glycemic responses assessed by the AUC of glucose levels did not differ between low-GI and high-GI SSBs. This is supported by other studies that also found a difference in insulin secretion between isomaltulose and sucrose/maltodextrin that prevented a difference in glucose levels.17, 34 It is therefore a major drawback of the GI-concept that it does not take insulin responses into account.35
During inactivity, 7-day consumption of beverages sweetened with low-GI isomaltulose led to a better preservation of insulin sensitivity when compared with high-GI SSBs. A continuous exposure to high insulin levels (hyperinsulinemia) has been shown to cause an impairment in insulin receptor function and thus to promote insulin resistance.6, 36 Higher day-long glycemic responses with high-GI SSBs might reflect lower inactivity-induced insulin sensitivity. In line with our findings, previous studies have shown an impaired insulin sensitivity and higher insulin secretion with a moderate decline in physical activity.25, 37
In a scientific consensus statement it is emphasized that low-GI diets are in particular relevant for prevention and management of diabetes in individuals with insulin resistance.38 Although some interventional studies suggest that the beneficial effects of a low-GI diet on glucose metabolism are more pronounced in predisposed individuals (for a review see Aston39), the current study has shown a beneficial effect of low-GI beverages in healthy fit men during only 1 week of physical inactivity.
Impact of low- vs high-GI SSBs on macronutrient oxidation
The present study shows that macronutrient oxidation was not affected by differences in insulin secretion and insulin sensitivity under energy balance conditions. Contrary to our findings, studies with weight loss and weight regain have shown a beneficial effect of low-GI diets on body weight regulation.23, 40, 41, 42 A low-GI diet is known to affect appetite regulation,43 but there are some studies that indicate that metabolic alterations may mediate the beneficial effects of a low-GI diet. In a study with seven healthy women 20-day low-GI versus high-GI carbohydrate diet (60% energy intake CHO) led to a higher fat oxidation in the fasted state.24 However, the study protocol was designed with exercise interventions and participants lost body weight with the low-GI but not with the high-GI diet.24 A previous study from our lab revealed that 2-weeks hypercaloric refeeding (+50% energy requirement) with a high-GI compared with a low-GI diet (50–65% energy) led to impaired basal fat oxidation and a tendency towards a higher regain in fat mass.23 By contrast, a carbohydrate-restricted weight loss diet improved fat oxidation, but led to a lower loss in body fat when compared with a high-carbohydrate diet.44
The bulk of literature focused on the impact of GI on acute postprandial substrate use, with the aim to show a greater reliance on fat oxidation with low-GI meals. Test carbohydrates were mostly provided in a solid form or in combination with other macronutrients.15, 16, 18, 45 Maltodextrin and isomaltulose are frequently used in sports beverages to support performance during endurance exercise.17 The present study revealed a lower increase in npRQtAUC-meal on inactivity with low-GI isomaltulose (Table 3) that was, however, explained by an unexpected higher baseline carbohydrate oxidation in the active phase (Figure 3). In contrast to our findings, Oosthuyse et al.17 observed a lower carbohydrate oxidation during exercise with continuously ingested isomaltulose beverages compared with a fructose–maltodextrin mixture in lean healthy men. In line with our findings, studies with sedentary individuals did not observe an impact of isomaltulose drinks (vs sucrose) consumed at breakfast on substrate use, even though insulin responses were lower with isomaltulose.19, 46 Other authors argue that GI-induced insulin responses in serum are not sufficient in magnitude and/or duration to affect macronutrient oxidation.47 The ratio between serum AUC insulin for the high- vs low-GI diet ranged in the most studies between 0.8 and 1.9 (ref. 47) and was 1.4 in the present study. It might also be possible that moderate differences in insulin levels without corresponding differences in glucagon responses (see results) might not be sufficient to modulate substrate use. In line with this, Galgani et al.48 did not find a relationship between insulin secretion and fuel selection during shorter terms (fasting/OGTT) in healthy non-diabetic participants. However, these authors revealed a relationship between 24-h RQ and day-long insulin response.48
Impact of physical inactivity on glucose metabolism and fuel selection
Inactivity affects a large majority of the population.25 The sharp reduction in habitual physical activity level (approximately −80%) led to impaired insulin sensitivity and to blunted basal and postprandial fat oxidation. In contrast, studies that induced training in sedentary individuals have shown an enhanced preference for fat oxidation in the fasted state, as well as an improved postprandial metabolic flexibility.49, 50, 51 Intervention studies that investigated the impact of detraining on fuel selection are rare. In line with our findings, Bergouignan et al.52 showed that 1-month detraining led to a blunted preference for fat oxidation in the fasted state26 and a decrease in postprandial metabolic flexibility. The present study showed that impairment in macronutrient oxidation with inactivity already occurred after 7 days. However, in a population that comprised healthy men with a very high habitual physical activity, mitochondrial capacity was likely to be high enough to compensate for adverse effect of hyperinsulinemia on metabolic flexibility.
Our results are applicable to short-term effects and cannot be broadened to chronic effects of low-GI or high-GI beverage consumption. The trial was implemented as nutritional intervention with controlled dietary intake and physical activity. Although all food was provided, ad libitum dietary intake resulted in a high day-to-day variance and some unintentional differences in energy and macronutrient intake with higher carbohydrate intake and lower protein intake during both inactive interventions compared with active baselines. Thus inactivity effects on glucose metabolism and fuel selection might also be partly due to a higher CHO intake. Participants consumed less energy and had a slight weight loss with the high-GI SSB but not with the low-GI SSB intervention. However, concomitant increase in body fat argues against a negative energy balance and adverse effects of high-GI maltodextrin plus sucrose on glucose metabolism would have only been diminished with lower energy intake. Finally, the interpretation of the inactivity effect is limited by the lack of a randomized cross-over design of low versus high activity.
In healthy men, 7-day consumption of high-GI SSB already led to impaired insulin sensitivity during physical inactivity. Low-GI isomaltulose sweetened beverage ameliorated this effect without affecting macronutrient oxidation.
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This study was funded by budgetary resources of the University Hohenheim. Isomaltulose (Palatinose) was kindly provided by Beneo GmbH (Mannheim, Germany) free of charge.
AB-W, JKh and JKr designed the research; JKh, JKr, HS-B and NB performed the research; JKh, JKr and A-BW analyzed the data; AB-W and JKh discussion of data; JKh and A-BW wrote the paper; JKh and AB-W had primary responsibility for final content. All authors read and approved the final manuscript.
The authors declare no conflict of interest.
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Kahlhöfer, J., Karschin, J., Silberhorn-Bühler, H. et al. Effect of low-glycemic-sugar-sweetened beverages on glucose metabolism and macronutrient oxidation in healthy men. Int J Obes 40, 990–997 (2016). https://doi.org/10.1038/ijo.2016.25
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