Metabolic response to a large starch meal after rest and exercise: comparison between men and women

Abstract

Background: Net whole-body and hepatic de novo lipogenesis could be more active in women than in men, but no comparison has been made between men and women in the two phases of the ovarian cycle after ingestion of a large carbohydrate meal.

Objective: We hypothesized that net whole-body de novo lipogenesis could be larger in women than men, and that glycogen and fat balance could be, respectively, lower and higher, following a large pasta meal ingested after rest or exercise.

Design: The metabolic response to a pasta meal (5 g dry weight/kg body mass) was studied in six men and six women (matched for age and BMI) in the follicular and luteal phases, following rest or exercise (90 min at 50% VO2max). Protein, glucose, and fat oxidation, and net whole-body de novo lipogenesis were computed for 10 h following ingestion of the meal using indirect respiratory calorimetry corrected for urea excretion.

Results: No net whole-body de novo lipogenesis was observed in any group in any situation (postrest and postexercise). When the meal was ingested following exercise, fat oxidation was significantly higher and glucose oxidation was significantly lower (P<0.05) than following the period of rest, and in a given experimental situation, the respective contributions of protein, fat, and glucose oxidation to the energy yield were similar in men and women in both phases of the cycle.

Conclusions: The contribution of substrate oxidation to the energy expenditure as well as fat and glycogen balance, and the effect of a previous exercise period, were similar in men and women in both phases of the cycle following ingestion of the large carbohydrate meal.

Introduction

Results from several studies indicate that a large carbohydrate meal does not result in a positive fat balance (Acheson et al, 1982, 1984, 1985, 1987; Hellerstein et al, 1991; Folch et al, 2001), particularly in the recovery period following exercise, when fat oxidation and glycogen storage have been shown to be favoured (Krzentowski et al, 1982; Bielinski et al, 1985; Broeder et al, 1991; Phelain et al, 1997; Folch et al, 2001). For example, in a recent study in nonobese men, we have shown that over the 8 h following ingestion of 300 g of starch, only 4 g of fat was synthesized when the subjects rested before the meal (Folch et al, 2001). When the subjects exercised before the meal, fat oxidation was maintained in the recovery period. As a consequence, a negative fat balance was observed in spite of the large excess of energy intake, with a preferential conversion of ingested glucose into glycogen.

Most studies of glucose disposal after an acute large carbohydrate meal (4.4–9.1 g glucose/kg) have been confined to men (Acheson et al, 1982, 1984, 1985, 1987; Hellerstein et al, 1991; Folch et al, 2001). In the studies conducted in women (Labayen et al, 1999; Bowden & McMurray, 2000), the amounts of carbohydrates ingested were much lower (1.7 g glucose/kg), and no comparison was made between the two phases of the ovarian cycle or between genders. However, over a 4-h period following a 2082 kJ (496 kcal) meal with 103 g of carbohydrates, Labayen et al (1999) observed that 5.3 g of fat was synthesized, in lean premenopausal women. When similar amounts of carbohydrates were ingested in men, fat balance remained negative (Krzentowski et al, 1983, 1984; Burelle et al, 1999; Korach et al, 2002). A positive fat balance has only been reported in men with ingestion of much larger amounts of carbohydrates (300–600 g with 0.5–9 g of fat synthesized) (Acheson et al, 1982, 1984, 1985,1987; Hellerstein et al, 1991; Folch et al, 2001). Faix et al (1993) also reported that hepatic de novo lipogenesis, monitored over 9 h with ingestion of 30 g/h of carbohydrates, was two-fold more active in women during the follicular phase of the ovarian cycle than in men. Taken together, these observations suggest that women could rely more on whole-body and/or hepatic de novo lipogenesis in the disposal of dietary carbohydrates, with, accordingly a more positive fat balance. In contrast, the replenishment of glycogen stores when carbohydrates are ingested following exercise could be smaller in women than men (Nicklas et al, 1989; Tamopolsky et al, 1995), particularly in the follicular phase of the cycle (Nicklas et al, 1989). These phenomena could contribute to the larger fat deposition in women than men, which is frequently reported in epidemiological studies (Molarius et al, 1999).

The purpose of the present study was, thus, to compare the metabolic response to carbohydrate ingestion after rest or exercise, in men and premenopausal women both in the mid-follicular and the mid-luteal phases of the ovarian cycle. Energy expenditure, substrate oxidation, and fat and glycogen balance were followed for 10 h after a large starch meal (5 g of pasta/kg body mass), ingested after a period of rest or of prolonged moderate exercise. Based on data from Labayen et al (1999) and Faix et al (1993), it was hypothesized that a larger positive fat balance will be observed following ingestion of the meal in women than in men, particularly in the mid-follicular phase of the cycle, while the replenishment of glycogen balance will be lower (Nicklas et al, 1989; Tamopolsky et al, 1995). It was also hypothesized that, as already shown in men (Folch et al, 2001), the exercise period before the meal will favour a negative fat balance and glycogen storage in women in both phases of the cycle.

Methods

Subjects

The experiment was conducted on six men and six pre menopausal women (Table 1). All the subjects were healthy and lean: percent body fat=15.5±3.7 and 28.3±2.3% for men and women, respectively (Impedancemetry, TBF5021, Tanita, Tokyo, Japan), and BMI <23 kg/m2. None of them were smokers, heavy drinkers, under medication, or had gained or lost weight over the past year (less than 1–2 kg changes). The subjects gave their informed written consent to participate in the study, which was approved by the Institutional Board on the use of human subjects in research. All subjects had a normal fasting plasma glucose concentration, and a normal response to an oral glucose load (Table 1). The women were not using oral contraceptives and were monitored using early-morning temperature for at least three menstrual cycles before entering the study, in order to verify that they were eumenorrheic with regular cycles lasting between 23 and 33 days (Hilgers & Bailey, 1980). They were then studied between days 6–10 (mid-follicular phase) and 17–25 following the first day of menses (mid-luteal phase), depending on the duration of the cycle. Significant differences (paired t-test, P<0.05) between the mid-follicular and mid-luteal phases of the cycle, respectively, for plasma FSH (5.9±0.1 and 3.3±0.1 IU/l), LH (6.3±0.2 and 3.1±0.2 IU/l), oestradiol (219±6 and 408±10 pmol/l), and progesterone concentrations (4.1±0.1 and 28.5±1.8 nmol/l) confirmed that the observations were made at the appropriate time in the cycle.

Table 1 Characteristics of the subjects, fasting plasma glucose concentration, and plasma glucose concentration at 120 min in response to a 75-g glucose load, and power output during exercise in each group

Experimental protocol

The subjects ingested a large pasta meal following a period of rest or exercise. They were then studied for 10 h. Experimental data concerning the rate of absorption of a large carbohydrate load are lacking. However, Acheson et al (1982) deemed reasonable the assumption that glucose from a 479-g carbohydrate meal was entirely absorbed over 5 h.

The men were studied twice, while the women were studied four times (twice in the mid-follicular and twice in the mid-luteal phase). The trials were separated by at least 7 days, and the first trial in premenopausal women was, at random, in the mid-follicular or the mid-luteal phase. During the 3 days preceding each test, the subjects refrained from exercising and from ingesting alcohol, and they were provided with prepackaged meals (147 kJ/kg/day) (35 kcal/kg/day) (Black et al, 1996) with 21% proteins, 56% carbohydrates, and 23% fat).

The subjects reported to the laboratory at 07.00 following a 12-h overnight fast and were provided with a standardized breakfast (25 kJ/kg (6 kcal/kg): 13% proteins, 45% carbohydrates, 42% fat), which was ingested between 07.00 and 07.30 (Table 2). The subjects, then either rested for 150 min in a comfortable semisupine position, or rested for 30 min, and then exercised from 08.00 to 09.30 on a cycle ergometer (Ergomeca, La Bayette, France) at a workload corresponding to 50% of the maximal aerobic workload. The order of presentation of the two situations was randomized among the subjects. As shown in Table 3, when compared to rest, the energy expenditure in response to exercise was three to four times higher, depending on the maximal aerobic power, with a much larger percent contribution to the energy yield from glucose than fat oxidation.

Table 2 Summary of the experimental protocol
Table 3 Energy expenditure and substrate oxidation between 07.30 and 09.30, at rest or exercise

Between 10.00 and 11.00, the subjects ingested a large starch meal (5 g of pasta dw per kg body mass; Panzani, Marseille, France) administered in five equal portions at 15-min intervals. The pasta was boiled for 7 min in water (100 g/l, with 7 g of table salt/l) and served with steamed onions and fresh tomatoes (60 g/100 g of dry pasta: 1 g of proteins; 5 g of carbohydrates; 0.2 g of fat; 109 kJ (26 kcal)), and salt and pepper. The composition of the pasta before cooking was as follows: 12.5% water, 70% starch (equivalent to 78 g of glucose and 1267 kJ/100 g (302 kcal/100 g)), 13.5% proteins (267 kJ/100 g (64 kcal/100 g)), and 4% fibres (12.5 g/100 g).

Measures and computations

Oxygen consumption (VO2) and carbon dioxide production (VCO2) (Tissot Spirometer, Warren-Collins Inc., Braintree, MA, USA; oxygen and carbon dioxide analysers MGA-1100, Marquette Electronics Inc., Milwaukee, WI, USA) were measured at regular intervals (10-min collection periods during exercise and 20-min collection periods every 60 min following the meal), and were corrected for protein oxidation (Livesey & Elia, 1988). For this purpose, protein oxidation and the associated amount of energy provided following the meal were computed from urea excretion in urine (Synchron Clinical System, CX7, Beckman, Anaheim, CA, USA). Protein oxidation before the meal was assumed to be 0.67 and 0.84 mg/kg fat-free mass/min at rest and in response to exercise (Folch et al, 2001). The tables developed by Elia and Livesey (1988) were, then, used for the computation of glucose and fat oxidation when the nonprotein respiratory quotient (NPRQ) was less than 1.0, or for the computation of glucose oxidation, and of the net amount of fat synthesized when the NPRQ was larger than 1.0. The balance of glycogen stores was computed as the difference between the amount of glucose ingested and oxidized, taking into account conversion of glucose into fat if any, and assuming that glucose provided by the meal was entirely absorbed over the observation period. Energy expenditure and substrate oxidation, and fat and glycogen balance were corrected for fat-free mass (FFM), in order to take into account differences in body size between men and women.

Blood samples

Blood samples (6–13 ml) were withdrawn at regular intervals from an indwelling catheter (Baxter Health Care Corp., Valencia, CA, USA) placed in an antecubital vein (immediately before ingesting the meal) for the measurement of plasma glucose, free fatty acids (Sigma Diagnostics, Sigma, Mississauga, Canada), and insulin concentrations (KTSP-11001, Immunocorp Sciences, Montreal, Canada).

Statistics

Data are presented as mean±s.e. The main effects of the experimental situation (ingestion postrest or postexercise) and of time were tested by analysis of variance for repeated measures, while comparisons between men and women in the mid-follicular and mid-luteal phase were made by analysis of covariance, with FFM as a covariable, in order to take into account the significant difference between men and women (Statistica package; StatSoft Inc., Tulsa, OK, USA). Newman–Keuls post hoc tests were used to identify the location of significant differences when the F ratios were significant (P<0.05).

Results

Protein oxidation was similar in men and women, and was similar when the meal was ingested after the period of rest and the period of exercise (Table 4), contributing 19.7–22.8% to the energy yield. The respiratory exchange ratio corrected for protein oxidation (NPRQ) markedly increased over the first 5 h following ingestion of the meal, but was back to the premeal values at the end of the observation period (Figure 1). In both experimental situations (postrest and postexercise), no significant difference was observed between men and women in both phases of the cycle. Premeal NPRQ values, as well as peak and average values, were slightly but significantly lower when the meal was ingested after the period of exercise than after the period of rest (Figure 1). In the middle of the observation period, the average NPRQ was high, particularly when the meal was ingested after the period of rest, but remained lower than 1.0, and a negative fat balance was observed in the three groups in both situations.

Table 4 Substrate oxidation and per cent contribution to the energy expenditure (% EE) over the 10 h following ingestion of the meal, postrest or postexercise
Figure 1
figure1

Changes in nonprotein respiratory quotient (NPQR) over the 10 h following ingestion of the meal after rest or exercise, in men and women in the two phases of the cycle (mean±s.e.; horizontal bars indicate the values different from those observed before the meal; P<0.05).

Ingestion of the meal resulted in a marked increase in total glucose oxidation (between 60 and 420 min) and a marked decrease in fat oxidation (between 60 and 480 min) (Figure 2). Overall substrate oxidation (and its contribution to the energy yield), during the 10-h observation period following the meal, and comparisons between gender and between the two experimental situation (postrest vs postexercise) are summarized in Table 4. In both experimental situations, energy expenditure, and glucose and fat oxidation were significantly higher in women in both phases of the cycle than in men. However, when the meal was ingested after the period of rest, the respective contributions of protein, glucose and fat oxidation to the energy yield were not significantly different in men and women in both phases of the cycle. In addition, when the meal was ingested after the period of exercise, glucose oxidation significantly decreased, while fat oxidation significantly increased in men as well as in women in both phases of the cycle. As a consequence, the respective contributions of protein, glucose, and fat oxidation to the energy yield over the 10-h observation period following the meal were also similar in men and women in both phases of the cycle.

Figure 2
figure2

Total glucose and fat oxidation in mg/kg FFM/min following ingestion of the meal after rest or exercise, in men and women in the two phases of the cycle, computed using indirect respiratory calorimetry corrected for protein oxidation (mean±s.e.; horizontal bars indicate the values different from those observed before the meal: main effect; P<0.05).

The net balance of glycogen stores over the 08.00–21.00 period (minus the 1-h meal period), and the 10-h period following the meal, was significantly lower when subjects exercised before the meal, and was similar in men and women (Table 5). The negative fat balance, computed as total fat oxidation for the period 08.00–21.00 (minus the 1-h meal period, and neglecting the small amount of fat in the meal: less than 1 g), was similar in men and women in the two phases of the cycle, and was significantly higher when subjects exercised before the meal (Table 5).

Table 5 Glycogen and fat balance over the 10-h observation period and over the 13-h observation period with rest or exercise before the meal

Plasma glucose and insulin concentrations before the meal (−60 min) were not significantly different in the two experimental situations (postrest and postexercise). In contrast, basal plasma-free fatty acid concentration was significantly higher following exercise. Plasma glucose and insulin concentrations both significantly increased above premeal values following ingestion of the meal, and remained elevated up to 420 and 300 min, respectively, following rest, and 240 min following exercise (Figure 3). Plasma-free fatty acid concentration sharply decreased and remained near zero between 60 and 360 min after both rest and exercise. Peak plasma glucose concentrations, which were observed at the end of the 1-h meal period, were significantly higher in all groups when subjects exercised than when remained at rest before ingestion of the meal. The responses of plasma glucose, insulin, and free fatty acid concentrations postexercise were not significantly different between men and women in the two phases of the cycle, although plasma insulin response was significantly higher in women than men when the meal was ingested after the period of rest, over the first 3 h following the meal.

Figure 3
figure3

Plasma glucose, insulin, and free fatty acid concentrations following ingestion of the meal after rest or exercise, in men and women in the two phases of the cycle (mean±s.e.; horizontal bars indicate the values significantly different from those observed before the meal; *significantly different from rest, significantly different from men; P<0.05).

Discussion

The purpose of the present experiment was to describe the metabolic response to a large dietary carbohydrate load, and the associated changes in energy expenditure, substrate utilization, and in glycogen and fat balance, in men and women who previously rested or exercised. Consistent data from several studies indicate that an acute large dietary carbohydrate load only results in a small positive fat balance, if any (Acheson et al, 1982, 1984, 1985, 1987; Hellerstein et al, 1991; Folch et al, 2001), particularly when ingested following prolonged exercise (Folch et al, 2001). However, most studies of net whole-body de novo lipogenesis and glucose disposal after an acute large carbohydrate meal have been confined to men (Acheson et al, 1982, 1984, 1985, 1987; Hellerstein et al, 1991; Folch et al, 2001), and no comparison has been made between genders. The two studies conducted in women provide conflicting results (Labayen et al, 1999; Bowden & McMurray, 2000). Bowden et al (2000) did not observe any conversion of glucose into fat in trained or untrained women over a 5-h period following ingestion of 94 g of carbohydrates. These findings are in line with data observed in men with similar amount of carbohydrates ingested (Krzentowski et al, 1983, 1984; Burelle et al, 1999; Korach et al, 2002). In contrast, Labayen et al (1999), following ingestion of 103 g of sucrose and lactose, have reported that 5.3 g of fat was synthesized over a 4-h period. A possible explanation for these conflicting results is that in the studies by Bowden et al (2000) and Labayen et al (1999), the women were not in the same phase of the ovarian cycle. Indeed, data from Faix et al (1993) indicate that hepatic de novo lipogenesis was similar in men and women in the luteal phase, but about two to three times more active during the follicular phase. Kenagy et al (1981), and Kim and Kalkhoff (1975) have also shown that oestradiol enhances triglyceride and VLDL synthesis in rat. Although these data are confined to hepatic de novo lipogenesis, it could be hypothesized that net whole-body de novo lipogenesis could also play a larger role in the disposal of an acute glucose load in women during the follicular than the luteal phase of the cycle than in men.

Results from the present experiment do not confirm this hypothesis. Following ingestion of the pasta meal, no net whole-body de novo lipogenesis was present in men or women in any of the phases of the cycle over the 10-h observation period. In fact, in both men and women, fat oxidation was maintained following the meal. When the meal was ingested after the period of rest, the amount of fat oxidized over the 10-h observation period was slightly but significantly higher in women than in men (0.45–0.48 vs 0.30 g/kg of FFM) but provided very similar percentages of the energy yield (21–22 vs 17%). As already observed by Bielinski et al (1985), Broeder et al (1991), Krzentowski et al (1982), Phelain et al (1997), Schneiter et al (1995), and in our own recent study (2001), in both men and women the exercise period before the meal increased fat oxidation following the meal. The contribution of fat oxidation to the energy yield increased from 17–22%, when the meal was ingested after the period of rest, to 27–30%, when it was ingested after the period of exercise. In contrast, glucose oxidation was significantly reduced by 14–16% when the meal was ingested following the period of exercise, its contribution to the energy yield being reduced from 57–60 to 50–52%. These changes in the metabolic response to a large carbohydrate meal cannot be related to the observed changes in plasma insulin concentration. Indeed, the response of plasma insulin concentration after the meal was similar following rest and exercise in women in both phases of the cycle, and was higher in men following exercise than rest, although this did not reach statistical significance (P=0.08) (Figure 3). Taken together, these data indicate that gender difference in fat balance in response to an acute carbohydrate load and/or changes in fat vs glucose oxidation cannot explain differences in fat deposition and the higher prevalence of obesity which is frequently observed in women (Molarius et al, 1999). However, ingestion of excess dietary carbohydrates for several days, in men, has been shown to result in a positive fat balance in lean (Acheson et al, 1988) as well as obese subjects (Horton et al, 1995; McDevitt et al, 2000). The same phenomenon could be present in women. In the present experiment, over a shorter period of observation, a negative fat balance was present (Table 5) (rest or exercise before the meal, and the 10-h period following the meal) because the amount of fat provided by the meal was negligible and a net conversion of glucose into fat was not present. The fat balance was more negative when the subjects exercised before the meal, not only because fat oxidation was larger during the exercise period than the corresponding period of rest (Table 3), but also because fat oxidation was favoured in the recovery period following exercise, in spite of the large amount of carbohydrate ingested. However, in the two experimental situations (rest or exercise), respectively, the negative fat balance was similar in men and women.

Glycogen storage as well as the metabolic consequences of the meal, and the effect of a previous exercise period on these responses, were also similar in men and women in both phases of the cycle. When the meal was ingested after the period of exercise, the responses of plasma glucose, insulin and free fatty concentrations were remarkably similar in men and women in both phases of the cycles. When the meal was ingested after the period of rest, the response of plasma insulin concentration was higher in women than men over the first 3 h of observation (Figure 3). This observation is not in line with data from Nilsson et al (2000) and Nuutila et al (1995), suggesting that insulin sensitivity assessed by the euglycaemic hyperinsulinaemic clamp technique is higher in women than men. However, there is apparently no data on possible gender difference in plasma insulin response to a large meal, when plasma glucose remains high for several hours. Glucose oxidation markedly increased following ingestion of the carbohydrate load (Figure 2), but remained lower when the meal was ingested after the period of exercise (Table 4). As a consequence, in this situation, glucose was spared and was available for replenishing glycogen stores. Over the 10-h observation period, assuming that all the glucose provided by the starch meal was absorbed, glycogen balance was significantly 21% higher in the recovery period from exercise. However, no significant difference was observed when the meal was ingested after rest or exercise, respectively, between men and women in both phases of the cycles. As suggested in the recent study by Tamopolsky et al (2001), the difference in glycogen storage reported between men and women following exercise could be caused by the difference in energy and carbohydrate intake, rather than by differences in the metabolic response to carbohydrate ingestion associated to progesterone and/or oestrogens. Results from the present study are in line with this hypothesis, and show that when provided with similar and large amount of carbohydrates following rest or exercise, glycogen storage was similar in men and women.

In summary, results from the present experiment indicate that the metabolic response to a large carbohydrate meal following rest and exercise was similar in men and women in both phases of the cycle. In both genders, net whole-body de novo lipogenesis did not play any role in the disposal of the glucose load. The larger contribution of fat oxidation to the energy yield, when the meal was ingested after a period of exercise, was also similar in men and women. Finally, glycogen balance over 13 h was higher when the meal was ingested following rest than exercise, but was similar in men and in women in both phases of the cycle.

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Acknowledgements

This study was supported by grants from the Natural Science and Engineering Research Council of Canada, and from the Fabricants Français de Pâtes Alimentaires, Groupe d'lntérêt Economique: Alimentation Recherche Nutrition (France).

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Correspondence to F Péronnet.

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Folch, N., Péronnet, F., Massicotte, D. et al. Metabolic response to a large starch meal after rest and exercise: comparison between men and women. Eur J Clin Nutr 57, 1107–1115 (2003). https://doi.org/10.1038/sj.ejcn.1601650

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Keywords

  • gender differences
  • insulin
  • calorimetry
  • fat balance
  • menstrual cycle

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