Objective:

To investigate whether the 'overnight second-meal effect' results in altered substrate oxidation during the postprandial period following breakfast and subsequent sub-maximal exercise in women.

Subjects/Methods:

Seven recreationally active women were recruited for the study. In each trial, participants were provided with their evening meal on day 1, which was composed of either high glycaemic index (HGI) or low glycaemic index (LGI) carbohydrates (CHO). On day 2, participants were provided with a standard HGI breakfast and then performed a 60 min run at 65% O_{2 max} 3 h later.

Results:

The incremental area under the curve (IAUC) for plasma glucose concentrations during the postprandial period following breakfast was greater in the HGI trial compared to the LGI trial (P<0.01). Similarly, the IAUC for serum insulin concentrations was greater in the HGI trial than the LGI trial (P<0.05). No differences in plasma free-fatty acids (FFA) or plasma glycerol concentrations were found between trials during the postprandial period. During subsequent exercise, there were no significant differences in substrate metabolism.

Conclusion:

The glycaemic index of an evening meal does not alter substrate oxidation at rest following breakfast or during subsequent submaximal exercise in women. This study provides further evidence for the overnight second-meal effect on glycaemic responses following a LGI mixed evening meal.

Introduction

The rate of carbohydrate (CHO) absorption after a meal, as predicted by the glycaemic index, has significant effects on the postprandial hormonal and metabolic responses (Ludwig, 2002). High glycaemic index (HGI) meals are associated with rapid hyperglycaemia and hyperinsulinaemia, which in many individuals, is followed by hypoglycaemia and the secretion of counterregulatory hormones. However, several factors can alter the glycaemic response to a given food or meal and an important factor is the characteristics of the previous meal. The concept of the second-meal effect has attracted interest in recent years (Liljeberg et al., 1999; Granfeldt et al., 2006; Nilsson et al., 2006) and can be briefly explained as the first of two consecutive CHO loads leading to improved glucose tolerance to the second (Axelsen et al., 1999). Improvements in glucose tolerance at a standard meal have been reported at lunchtime following a low glycaemic index (LGI) breakfast compared to when an energy-matched HGI breakfast is consumed (Liljeberg et al., 1999; Liljeberg and Bjorck, 2000). The GI of an evening meal has also been shown to significantly alter the glycaemic response to a standard breakfast the following morning in both healthy male subjects (Wolever et al., 1988; Stevenson et al., 2005) and those with type II diabetes (Axelsen et al., 1999).

In sport and exercise nutrition, LGI pre-exercise meals are often recommended to maintain plasma glucose concentrations and free-fatty acids (FFA) during exercise as a consequence of a lower insulin response in the period before exercise (Thomas et al., 1991). Despite this, many athletes chose not to consume LGI foods due to the gastrointestinal discomfort that may occur. If a LGI meal consumed the evening before exercise can reduce the hyperglycaemia and hyperinsulinaemia following a standard HGI breakfast, a similar effect may be achieved to when a LGI pre-exercise meal is consumed. This was recently investigated in a study from our laboratory using healthy male subjects (Stevenson et al., 2005). Despite improved glucose tolerance to a standard breakfast following a LGI evening meal, no differences in substrate oxidation were reported either during the 3 h postprandial period following breakfast or during subsequent exercise compared to when a HGI evening meal was consumed.

Surprisingly, there is very little data on the glycaemic responses to HGI and LGI meals in women despite the fact that women are more likely to adopt a LGI diet for weight loss purposes. A recently study by Basu et al. (2006) demonstrated that sex differences do exist in postprandial glucose metabolism. The authors reported that, following a mixed CHO meal, both postprandial glucose and insulin concentrations were greater in young women than men. Several studies have also reported that gender differences exist in both glucose kinetics during submaximal exercise (Horton et al., 2006) and the relative utilization of CHOs and lipids as fuel sources (Tarnopolsky et al., 1995; Knechtle et al., 2004; Venables et al., 2005). Although some studies have reported no differences in substrate oxidation during exercise between men and women (Mittendorfer et al., 2002; Roepstorff et al., 2002), at present, there is insufficient evidence to warrant generalizing that research findings about male subjects also apply to female subjects.

Glycaemic characteristics of meals that are commonly consumed are also lacking in the GI literature, despite the fact that LGI diets are now being recommended to the general public as an effective weight loss method. Therefore the purpose of the present study was to investigate whether the acute effects of a LGI meal persist overnight in women and whether this effect is large enough to alter metabolism and substrate oxidation both during the postprandial period following breakfast and during subsequent submaximal exercise.

Methods

Subjects

Seven female recreational athletes participated in this study. Their mean (s.d.) age, height, weight and were 24.43.4 years, 170.01.0 cm, 59.97.3 kg and 52.24.4 mlkg^{- 1} min^{- 1} respectively. All subjects were eumenorrheic. A criterion for inclusion in the study was that participants ran regularly and were able to run for one hour continuously at about 65% . Loughborough University Ethical Advisory Committee approved the protocol and all subjects gave their written informed consent.

Preliminary measurements

Following familiarization with treadmill running and experimental procedures, subjects undertook two preliminary tests in order to determine: (1) the relationship between running speed and oxygen uptake using a 16 min incremental test and (2) their using an uphill incremental treadmill test to exhaustion. All preliminary tests were conducted according to procedures described previously (Williams et al., 1990). On the basis of the results of the two preliminary tests, the running speed equivalent to 65% of each subject's was determined.

Experimental design

Each subject participated in two experimental trials separated by at least 1 week. During the first trial, four women were in the follicular phase of the menstrual cycle and three in the luteal phase. During trial two, three women were in the follicular phase of the cycle and four in the luteal phase. The experimental testing protocol was completed over a 2-day period. On day 1, subjects were provided with an evening meal consisting of either HGI or LGI CHO. On day 2, subjects arrived at the laboratory following a 13 h overnight fast and were provided with a standard HGI breakfast. Following ingestion of breakfast, subjects remained in the laboratory at rest for 3 h. At the end of the 3 h postprandial period, subjects completed a 60 min run at 65% .

All trials were performed at the same time of day and under similar experimental and environmental conditions. The same treadmill was also used throughout the experiment (Technogym Run Race Treadmill, 47035, Gambettoio, Italy) For 2 days before the first trial, the subjects recorded their diet and exercise routine so that it could be repeated before trial 2 to minimize differences in pretesting intramuscular substrate concentrations between experimental trials. Subjects were advised to maintain their normal training schedule during the study but to abstain from any vigorous exercise in the 24 h period before the two experimental trials. During this period they were also instructed to avoid alcohol, caffeine and smoking.

Protocol

On day 1 of the experimental protocol, subjects were asked to record their food intake at breakfast and lunch. They were instructed not to consume any food after 1600 h and were then provided with their test meal at 1900 h. After ingestion of this meal, subjects were allowed water only until the following morning.

On day 2 of the experiment each subject arrived in the laboratory at 0800 h. On arrival, subjects completed the necessary health and consent forms and were then asked to void before mass was obtained (Avery, England). A cannula (Venflon 18G, Becton Dickinson Ltd, Helsingborg Sweden) was then inserted into an antecubital vein and connected to a three-way stopcock (Connecta Ltd, Helsingborg, Sweden) with a 10 cm extension tube for blood sampling. The cannula was kept patent by flushing with saline solution immediately after the cannula was inserted and after blood sampling. Once the cannula had been in place for 15 min, a fasting 10 ml venous blood sample and a 5 min resting expired air sample were collected and then the participants were provided with the standard HGI breakfast. Subjects were asked to consume the breakfast within 15 min and then the 3 h postprandial period began.

During the postprandial period, subjects remained in the laboratory at rest. Ten millitres venous blood samples and 5 min expired air samples were taken 15, 30, 60, 90, 120 and 180 min after breakfast. During each collection of expired air, ratings of gut fullness and hunger were recorded using 6–20 scales adapted from the Borg Scale (Borg, 1973) so that the anchor terms were 'not full' to 'very, very full' and 'not hungry' to 'very, very hungry'. Subjects were instructed not to eat anything other than the food provided for them. No extra drinks, apart from water, were permitted.

Following the 3 h postprandial period, subjects were weighed and then changed into running clothes. A short-range telemeter (Technogym, Gambettoio, Italy) heart rate (HR) monitor was then attached to the subject to monitor HR. Subjects completed a 5 min warm-up at 60% and then the treadmill speed was increased to a speed that represented 65% of the individuals . All subjects then completed 60 min running at this speed. The running speed ranged from 8 to 10.5 km h^{- 1}. A 1 min expired air sample was collected after 5 min of running to check the intensity of the exercise was correct. The treadmill speed was adjusted if necessary so that the intensity represented 65% of the individuals . Further expired air samples were collected for 1 min every 15 min throughout the exercise protocol. Following each expired air sample, a 10 ml blood sample was also collected. Rating of perceived exertion was recorded at 15 min intervals and HR was monitored frequently throughout the run.

Water was available ad libitum during trial 1 however the volume was measured and recorded and matched in trial 2. At the end of the run, subjects removed surface sweat and were weighed in minimal clothing. All trials were performed at the same time of day and under similar experimental and environmental conditions. The same treadmill was also used throughout the experiment (Technogym Run Race Treadmill, 47035, Gambettoio, Italy).

Ambient temperature and relative humidity were recorded every 30 min using a hygrometer (Zeal, London, UK) during the main trials. Temperature was maintained between 21 and 23°C and humidity was between 50 and 60% .

Test meals

Isocaloric evening meals consisting of HGI or LGI CHO foods were provided for each subject on day 1 of each trial. On day 2, a standard HGI breakfast was consumed in the laboratory (Table 1). The amount of CHO provided in each meal was 2 g CHOkg^{- 1} BM. The evening meals were not however matched for non-starch polysaccharide (NSP) content with the LGI evening meal containing 8.9 g NSP and the HGI evening meal containing 4.0 g NSP (both values based on a breakfast for a 60 kg individual). Other foods were added to the diet (e.g. margarine, cheese and lettuce) to make them more palatable; however the same quantity was used in both diets. The nutritional content of each meal was calculated from information provided by the manufacturer. The GI of each meal was calculated from the weighted means of the GI values for the component foods (Wolever and Jenkins, 1986). The calculated GI for the high- and low-GI evening meals were 72 and 34, respectively and the GI of the standard breakfast was calculated to be 77.

Table 1 - Characteristics of the test meals (for a 60 kg person).

Full table

Sample collection and analysis

Expired air samples were collected using the Douglas Bag Method. During rest, 5 min expired air samples were collected and during exercise collections were for 1 min. Each sample was collected via a low resistance one-way respiratory valve and a lightweight Falconia tubing (Baxter, Woodhouse and Taylor, UK). The samples were analysed for oxygen and carbon dioxide content by passing a small sample through a gas analyser (Servomex 1440, England). The analyser was calibrated before use against nitrogen and a mixture of gases of known concentration (16% oxygen and 4% carbon dioxide) (British Oxygen Company, UK). The remaining volume in the Douglas Bag was then measured using a dry gas metre (Harvard Apparatus Ltd., Edenbridge, UK) and the temperature of the gas was measured at the same time using a thermometer (Edale Instruments, model C, UK). Oxygen uptake () and carbon dioxide production () were calculated using the method described previously (Williams et al., 1990). The subjects remained seated for all expired air samples throughout the postprandial period. Substrate oxidation rates were calculated using the following non-protein stoichiometric equations (Frayn, 1983):

At each sampling point, 10 ml of blood was collected and 5 ml of whole blood was immediately dispensed into an ethylenediaminetetraacetic acid tube. Haemoglobin (Hb) concentration was determined using the cyanmethaemoglobin method (Boehringer Mannheim, Mannheim Germany) (2 20 l) and haematocrit (Hct) values were determined in triplicate on samples of whole blood by microcentrifugation (Hawksley Ltd, Lancing, Sussex, UK). Changes in plasma volume were estimated from changes in Hb concentrations and Hct values, as described by Dill and Costill, (1974). Blood lactate concentration was analysed by a photometric method using a spectrophotometer (Shimazu mini 1240, Shimazu Corp., Kyoto, Japan). Plasma samples were obtained by centrifugation of the remaining whole blood for a period of 10 min at 4000 r.p.m. and 4°C. The aliquoted plasma was then stored at - 85°C for later analysis of FFA (ASC-ACOD method, Wako NEFA C; Wako, Neuss, Germany), glucose (GOD-PAP method, Randox, Ireland) and glycerol (Randox, Ireland) using an automatic photometric analyser (Cobas-Mira plus, Roche, Basel, Switzerland). The remaining whole-blood sample was dispensed into a non-anticoagulant tube and left to clot for 45 min. Serum samples were then obtained after centrifugation at 4000 r.p.m. for 10 min at 4°C. The aliquoted serum was stored at - 85°C and later analysed for insulin (Coat-A-Count Insulin ICN Ltd, Eschwege, Germany) by radio immunoassay using a gamma counter (Cobra 5000, Packard Ltd, Boston, MA, USA). Pre-trial urine samples were measured for osmolality using a cryoscopic osmometer (Gonometer 030, Gonotec, Germany) and adequate hydration was assumed for osmolality values below 900 mosmolkg^{- 1} (Shirreffs and Maughan, 1998).

Statistical analysis

Analysis of variance (ANOVA) for repeated measures on two factors (experimental treatment and time) was used to analyse differences in the physiological and metabolic responses in both trials. Preliminary analysis was carried out to investigate whether a phase of menstrual cycle diet interaction existed in the results. No significant interaction was found therefore results were analysed irrespective of menstrual cycle phase. If a significant interaction was obtained following ANOVA, a Holm–Bonnferoni step-wise post hoc test was utilized to determine the location of the variance. Differences were considered significant at P<0.05. All results are presented as means.e.m.

Results

Plasma glucose and serum insulin

There was a main trial effect for plasma glucose concentrations to be higher throughout the postprandial period in the HGI trial compared to the LGI trial (P<0.05) (Figure 1). Following ingestion of the standard HGI breakfast, plasma glucose concentrations rapidly increased and peaked at 15 min during the postprandial period in both trials. Plasma glucose concentrations then declined throughout the rest of the postprandial period. The incremental area under the curve (IAUC) for plasma glucose during the postprandial period following breakfast was greater in the HGI trial than the LGI trial (18541 mmol l^{- 1} 180 min and 11029 mmol l^{- 1} 180 min respectively) (P<0.01) thus, confirming the main trial effect. Throughout the run, plasma glucose concentrations were maintained between 4.5 and 5 mmol l^{- 1} in the LGI trial. In the HGI trial, plasma glucose concentrations increased throughout the run to approximately 6 mmol l^{- 1} at the end of the 60 min however, there were no significant differences between the trials.

Figure 1.

Plasma glucose concentrations (mmol l^{- 1}) during the HGI and LGI trials (means.e.m.). Two-way ANOVA showed a significant main effect of trial for plasma glucose concentrations to be higher in the HGI trial compared to the LGI trial (P<0.05).

Full figure and legend (13K)

There was also a main trial effect for serum insulin concentrations to be higher throughout the postprandial period following the standard breakfast when the HGI evening meal was consumed compared to when the LGI evening meal was consumed (P<0.05) (Figure 2). Following ingestion of breakfast, serum insulin concentrations increased rapidly and peaked at 15 min during the postprandial period in both trials. Serum insulin concentrations then declined throughout the rest of the postprandial period and remained at baseline levels throughout the 60 min run in both trials. The IAUC for serum insulin during the postprandial period was greater in the HGI trial than the LGI trial (133742115 lU ml^{- 1} 180 min and 109381484 lU ml^{- 1} 180 min respectively) (P<0.05) again confirming the main trial effect.

Figure 2.

Serum insulin concentrations (lU.ml^{- 1}) during the HGI and LGI trials (means.e.m.). Two-way ANOVA showed a significant main effect of trial for serum insulin concentrations to be higher in the HGI trial compared to the LGI trial (P<0.05).

Full figure and legend (12K)

Plasma FFA and glycerol

Before the ingestion of the standard breakfast, FFA concentrations were higher in the HGI trial compared to the LGI trial (P<0.05). Following ingestion of breakfast, plasma FFA concentrations were suppressed in both trials and remained suppressed throughout the postprandial period. During the submaximal exercise bout, FFA concentrations increased with time but again, there were no differences between trials (Figure 3). Plasma glycerol concentrations showed a similar response to that of plasma FFA and there were no differences between the trials (Figure 4).

Figure 3.

Plasma FFA concentrations (mmol l^{- 1}) during the HGI and LGI trials (means.e.m.). Two-way ANOVA showed a significant GI - - time interaction (P<0.05). Bonnferroni correction was used to analyse significance at specific time points. ^*HGI trial significantly higher than LGI trial (P<0.05.).

Full figure and legend (12K)

Figure 4.

Plasma glycerol concentrations (mol l^{- 1}) during the HGI and LGI trials (means.e.m.). No significant differences following a two-way ANOVA.

Full figure and legend (12K)

Blood lactate

In both trials, blood lactate concentrations increased slightly after ingestion of the HGI breakfast but there were no differences between the trials. During the exercise bout blood lactate concentrations increased in both trials but remained between 1 and 2 mmol l^{- 1} throughout the run (Figure 5).

Figure 5.

Blood lactate concentrations (mmol l^{- 1}) during the HGI and LGI trials (means.e.m.). No significant differences following a two-way ANOVA.

Full figure and legend (13K)

Respiratory exchange ratio (RER) and estimated CHO and fat oxidation rates

There were no significant differences between trials in the RER (Table 2) and therefore the estimated rate of CHO (Figure 6) and fat oxidation (Figure 7) during either the postprandial period or the 60 min run.

Figure 6.

Estimated rate of CHO oxidation (g min^{- 1}) during the HGI and LGI trials (means.e.m.). No significant differences following a two-way ANOVA.

Full figure and legend (11K)

Figure 7.

Estimated rate of fat oxidation (g.min^{- 1}) during the HGI and LGI trials (means.e.m.). No significant differences following a two-way ANOVA.

Full figure and legend (12K)

Table 2 - VO₂, VCO₂ and the RER during the HGI and LGI CHO trials (means.e.m.).

Full table

Gut fullness and hunger scales

Throughout the postprandial period following the standard breakfast, ratings of gut fullness were higher in the LGI trial compared to the HGI trial (P<0.05). No differences in gut fullness were observed during the subsequent 60 min run. There were no significant differences in feelings of hunger but a trend for ratings to be higher in the HGI trial (Table 3).

Table 3 - (HR), RPE, GF and hunger scale ratings during the HGI and LGI CHO trials (means.e.m.).

Full table

Plasma volume changes and hydration status

There was minimal change in plasma volume throughout the postprandial period in both trials. Plasma volume was significantly decreased by the end of the exercise bout (P<0.05) but there were no differences between the trials. At the start of each trial, all participants had a urine osmolality that suggested that they were well hydrated (62866 and 487107 mosmol kg^{- 1} in the HGI and LGI trials respectively) (NS).

Discussion

The present study confirms that an overnight second meal effect occurs in healthy female subjects who consumed a LGI mixed evening meal compared to when an energy-matched HGI mixed meal was consumed. Despite the lower glycaemic and insulinaemic responses during the postprandial period following breakfast in the LGI trial, no differences in substrate utilization were observed during the postprandial period following breakfast or during subsequent submaximal exercise. This is in agreement with results reported previously in healthy male subjects (Stevenson et al., 2005). Similarly, no differences in FFA, glycerol or lactate concentrations were reported between the trials. Several studies have reported higher rates of fat oxidation during exercise when a LGI pre-exercise meal or food is consumed (Thomas et al., 1991; Wee et al., 1999; Wu et al., 2003; Stevenson et al., 2006). Reduced hyperinsulinaemia during the postprandial period following the LGI meal reduces the suppression of fat oxidation compared to when a HGI meal is consumed. This allows a shift in substrate utilization toward fat oxidation during the subsequent exercise as well as providing a sustainable source of CHO (Wu et al., 2003). The results of the present therefore show that a LGI meal needs to be eaten in the 2–3 h before the exercise bout to achieve this shift in substrate utilization.

Previous studies have reported improved glucose tolerance following a single LGI meal or food either 4 h later (Jenkins et al., 1982; Liljeberg et al., 1999; Liljeberg and Bjorck, 2000) or the next day in healthy male subjects (Wolever et al., 1988) and type II diabetics (Axelsen et al., 1999). Neither study however investigated whether this phenomenon occurred in women alone. Indeed, many of the acute studies investigating the metabolic effects of the glycaemic index of pre-exercise meals have used male subjects. The lack of data on glycaemic and insulinaemic responses to CHO with different GI values in women suggests that in many cases, the results from studies on male subjects are being directly applied to the female population. Several studies have shown that differences in substrate oxidation exist both at rest and during exercise between male and female subjects (Horton et al., 1998; Mittendorfer et al., 2002; Steffensen et al., 2002). The results of the present study are however very similar to those reported previously in male subjects who undertook exactly the same protocol (Stevenson et al., 2005). There appear to be no gender differences in the metabolic responses to the standard breakfast or subsequent exercise in either of the trials. Further research is necessary to investigate gender differences in both postprandial and exercise metabolism.

The exact mechanism behind the so-called overnight 'second meal effect' is still unclear. It has been suggested that the GI of an evening meal per se can predict the glucose response to a standard test meal the following morning (Wolever et al., 1988). However, in a recent study, Granfeldt et al. (2006) reported that a LGI meal per se was not enough to reduce the glycaemic response to a standard test meal the next morning. Only a LGI meal rich in indigestible CHO significantly lowered glucose and insulin responses to a subsequent meal. Indigestible CHO pass through the small intestine and into the colon undigested and become substrate for fermentation by colonic bacteria (Rumessen, 1992). The resulting formation of short-chain fatty acids (SCFA) is thought to have beneficial effects on glucose metabolism, particularly by modifying the gastric emptying rate (Cherbut, 2003). The NSP content of the LGI meal in the present study was approximately twice that of the HGI evening meal. It is reasonable to suggest therefore that colonic fermentation of indigestible CHO may have played a role in the reduced glycaemic and insulinaemic response to the standard breakfast in the present study. It is important to note that there is no breath hydrogen data to support this suggestion and therefore simply collecting expired air samples to measure substrate oxidation may not be sufficient to provide a full picture of metabolism following a high NSP, LGI meal. Fasting FFA concentrations were also lower in the LGI trial compared to the HGI trial before the standard test breakfast was consumed. This finding is in agreement with other studies that have investigated the overnight second meal effect (Thorburn et al., 1993; Nilsson et al., 2006). The production of SCFA has been shown to reduce circulating venous FFA concentrations (Wolever et al., 1991). This consequently decreases hepatic glucose output, hence reducing the overall glycaemic response.

Interestingly, subjective ratings of gut fullness were reported to be higher in the postprandial period following breakfast in the LGI trial than in the HGI trial. This is despite the fact that the breakfast was exactly the same in both trials. Several studies have reported that the consumption of LGI foods reduces hunger and/or promotes satiety relative to consumption of HGI foods in the hours following consumption of the meal (Ludwig et al., 1999; Ball et al., 2003; Warren et al., 2003; Wu et al., 2003). The effect of glycaemic CHO on food intake appears to be related to their effects on blood glucose (Anderson and Woodend, 2003). However, the release of putative satiety peptides, mediated by the intensity and length of interaction of CHO in the gastrointestinal tract appears to be a crucial component of mechanisms initiating and sustaining satiety (Anderson and Woodend, 2003).

In the present study, no differences in substrate oxidation were reported during the postprandial period following breakfast despite the reduced glycaemic and insulinaemic response to breakfast in the LGI trial. This is in agreement with previous studies that have investigated the effect of a single pre-exercise meal or food with differing GI values on substrate metabolism during exercise (Wee et al., 1999; Wu et al., 2003; Stevenson et al., 2005). It has been suggested that the chronic intake of a LGI diet results in changes in fuel partitioning and substrate oxidation due to reduced insulinaemia in the postprandial period. We have reported previously that fat oxidation during the postprandial period following a second LGI meal was significantly higher compared to when two HGI meals are consumed (Stevenson et al., 2005). It is therefore likely that a 3 h postprandial period is of insufficient duration to highlight differences in substrate oxidation rate during the postprandial period.

In conclusion, the consumption of a LGI evening meal can improve glucose tolerance at a second meal following an overnight fast in women. Despite reduced hyperglycaemia and hyperinsulinaemia in the postprandial period following the standard breakfast in the LGI trial compared to the HGI trial, no differences in substrate utilization were reported either during the postprandial period following breakfast or during subsequent exercise. It is therefore evident that LGI foods need to be consumed in the hours before exercise to have an effect on substrate metabolism. Further research is necessary to understand the metabolic responses to foods with different GI's in women so that accurate dietary advice can be provided.

References

1. Anderson GH, Woodend D (2003). Effect of glycemic carbohydrates on short-term satiety and food intake. Nutr Rev 61 (5 Pt 2), S17–S26. | Article | PubMed | ISI |
2. Axelsen M, Arvidsson Lenner R, Lonnroth P, Smith U (1999). Breakfast glycaemic response in patients with type 2 diabetes: effects of bedtime dietary carbohydrates. Eur J Clin Nutr 53, 706–710. | Article | PubMed | ChemPort |
3. Ball SD, Keller KR, Moyer-Mileur LJ, Ding YW, Donaldson D, Jackson WD (2003). Prolongation of satiety after low versus moderately high glycemic index meals in obese adolescents. Pediatrics 111, 488–494. | Article | PubMed | ISI |
4. Basu R, Dalla Man C, Campioni M, Basu A, Klee G, Toffolo G et al. (2006). Effects of age and sex on postprandial glucose metabolism: differences in glucose turnover, insulin secretion, insulin action, and hepatic insulin extraction. Diabetes 55, 2001–2014. | Article | PubMed | ChemPort |
5. Borg GA (1973). Perceived exertion: a note on 'history' and methods. Med Sci Sports 5, 90–93. | PubMed | ChemPort |
6. Cherbut C (2003). Motor effects of short-chain fatty acids and lactate in the gastrointestinal tract. Proc Nutr Soc 62, 95–99. | Article | PubMed | ISI | ChemPort |
7. Dill DB, Costill DL (1974). Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37, 247–248. | PubMed | ISI | ChemPort |
8. Foster-Powell K, Holt SH, Brand-Miller JC (2002). International table of glycemic index and glycemic load values. Am J Clin Nutr 76 (1), 5–56. | PubMed | ISI | ChemPort |
9. Frayn KN (1983). Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 55, 628–634. | PubMed | ISI | ChemPort |
10. Granfeldt Y, Wu X, Bjorck I (2006). Determination of glycaemic index; some methodological aspects related to the analysis of carbohydrate load and characteristics of the previous evening meal. Eur J Clin Nutr 60, 104–112. | Article | PubMed | ISI | ChemPort |
11. Horton TJ, Grunwald GK, Lavely J, Donahoo WT (2006). Glucose kinetics differ between women and men, during and after exercise. J Appl Physiol 100, 1883–1894. | Article | PubMed | ChemPort |
12. Horton TJ, Pagliassotti MJ, Hobbs K, Hill JO (1998). Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol 85, 1823–1832. | PubMed | ChemPort |
13. Jenkins DJ, Wolever TM, Taylor RH, Griffiths C, Krzeminska K, Lawrie JA et al. (1982). Slow release dietary carbohydrate improves second meal tolerance. Am J Clin Nutr 35, 1339–1346. | PubMed | ISI | ChemPort |
14. Knechtle B, Muller G, Willmann F, Kotteck K, Eser P, Knecht H (2004). Fat oxidation in men and women endurance athletes in running and cycling. Int J Sports Med 25, 38–44. | Article | PubMed | ChemPort |
15. Liljeberg H, Bjorck I (2000). Effects of a low-glycaemic index spaghetti meal on glucose tolerance and lipaemia at a subsequent meal in healthy subjects. Eur J Clin Nutr 54, 24–28. | Article | PubMed | ISI | ChemPort |
16. Liljeberg HG, Akerberg AK, Bjorck IM (1999). Effect of the glycemic index and content of indigestible carbohydrates of cereal-based breakfast meals on glucose tolerance at lunch in healthy subjects. Am J Clin Nutr 69, 647–655. | PubMed | ISI | ChemPort |
17. Ludwig DS (2002). The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 287, 2414–2423. | Article | PubMed | ISI | ChemPort |
18. Ludwig DS, Majzoub JA, Al-Zahrani A, Dallal GE, Blanco I, Roberts SB (1999). High glycemic index foods, overeating, and obesity. Pediatrics 103, E26. | Article | PubMed | ChemPort |
19. Mittendorfer B, Horowitz JF, Klein S (2002). Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab 283, E58–E65. | PubMed | ChemPort |
20. Nilsson A, Granfeldt Y, Ostman E, Preston T, Bjorck I (2006). Effects of GI and content of indigestible carbohydrates of cereal-based evening meals on glucose tolerance at a subsequent standardised breakfast. Eur J Clin Nutr 60, 1092–1099. | Article | PubMed | ChemPort |
21. Roepstorff C, Steffensen CH, Madsen M, Stallknecht B, Kanstrup IL, Richter EA et al. (2002). Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab 282, E435–E447. | PubMed | ChemPort |
22. Rumessen JJ (1992). Hydrogen and methane breath tests for evaluation of resistant carbohydrates. Eur J Clin Nutr 46 (Suppl 2), S77–S90. | PubMed | ISI |
23. Shirreffs SM, Maughan RJ (1998). Urine osmolality and conductivity as indices of hydration status in athletes in the heat. Med Sci Sports Exerc 30, 1598–1602. | Article | PubMed | ChemPort |
24. Steffensen CH, Roepstorff C, Madsen M, Kiens B (2002). Myocellular triacylglycerol breakdown in females but not in males during exercise. Am J Physiol Endocrinol Metab 282, E634–E642. | PubMed | ChemPort |
25. Stevenson E, Williams C, Mash L, Phillips B, Nute M (2006). Influence of high-carbohydrate mixed meals with different glycemic indexes on substrate utilization during subsequent exercise in women. Am J Clin Nutr 84, 354–360. | PubMed | ChemPort |
26. Stevenson E, Williams C, Nute M (2005). The influence of the glycaemic index of breakfast and lunch on substrate utilisation during the postprandial periods and subsequent exercise. Br J Nutr 93, 885–893. | Article | PubMed | ChemPort |
27. Stevenson E, Williams C, Nute M, Swaile P, Tsui M (2005). The effect of the glycemic index of an evening meal on the metabolic responses to a standard high glycemic index breakfast and subsequent exercise in men. Int J Sport Nutr Exerc Metab 15, 308–322. | PubMed | ChemPort |
28. Tarnopolsky MA, Atkinson SA, Phillips SM, MacDougall JD (1995). Carbohydrate loading and metabolism during exercise in men and women. J Appl Physiol 78, 1360–1368. | PubMed | ChemPort |
29. Thomas DE, Brotherhood JR, Brand JC (1991). Carbohydrate feeding before exercise: effect of glycemic index. Int J Sports Med 12, 180–186. | PubMed | ISI | ChemPort |
30. Thorburn A, Muir J, Proietto J (1993). Carbohydrate fermentation decreases hepatic glucose output in healthy subjects. Metabolism 42, 780–785. | Article | PubMed | ISI | ChemPort |
31. Venables MC, Achten J, Jeukendrup AE (2005). Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J Appl Physiol 98, 160–167. | Article | PubMed |
32. Warren JM, Henry CJ, Simonite V (2003). Low glycemic index breakfasts and reduced food intake in preadolescent children. Pediatrics 112, e414. | Article | PubMed | ISI |
33. Wee SL, Williams C, Gray S, Horabin J (1999). Influence of high and low glycemic index meals on endurance running capacity. Med Sci Sports Exerc 31, 393–399. | Article | PubMed | ChemPort |
34. Williams C, Nute MG, Broadbank L, Vinall S (1990). Influence of fluid intake on endurance running performance. A comparison between water, glucose and fructose solutions. Eur J Appl Physiol Occup Physiol 60, 112–119. | Article | PubMed | ChemPort |
35. Wolever TM, Jenkins DJ (1986). The use of glycemic index in predicting the blood glucose response to mixed meals. Am J Clin Nutr 43, 167–172. | PubMed | ISI | ChemPort |
36. Wolever TM, Jenkins DJ, Ocana AM, Rao VA, Collier GR (1988). Second-meal effect: low-glycemic-index foods eaten at dinner improve subsequent breakfast glycemic response. Am J Clin Nutr 48, 1041–1047. | PubMed | ISI | ChemPort |
37. Wolever TM, Spadafora P, Eshuis H (1991). Interaction between colonic acetate and propionate in humans. Am J Clin Nutr 53, 681–687. | PubMed | ISI | ChemPort |
38. Wu CL, Nicholas C, Williams C, Took A, Hardy L (2003). The influence of high-carbohydrate meals with different glycaemic indices on substrate utilisation during subsequent exercise. Br J Nutr 90, 1049–1056. | Article | PubMed | ChemPort |

Acknowledgements

We thank the women who participated in this study. EJS produced the original study design, performed the laboratory investigations and biochemical analysis, undertook the statistical data analysis, and wrote the first draft of the article. MLN, LH and OW assisted with the laboratory investigations and biochemical analysis. CW supervised the data collection, contributed to the data interpretation and revised the article. None of the authors had any conflicts of interest.