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1 From the Laboratoire de Bioénergétique Fondamentale et Appliquée, Université Joseph Fourier, Grenoble, France (MK-A, HR, DB, and XL); the Service de Nutrition Parentérale, Centre Hospitalier Universitaire, Grenoble, France (HR, DB, and XL); the Département de Kinésiologie, Université de Montréal, Canada(FP); and the Groupe de Recherches Appliquées en Phytotechnologie, Commission de lÉnergie Atomique, Cadarache, France (MP).
2 Supported by grants from the Natural Sciences and Engineering Research Council of Canada and the Ministère de lAgriculture and the Ministère de la Recherche of France (Programme Aliment-demain). 3 Reprints not available. Address correspondence to F Péronnet, Département de Kinésiologie, Université de Montréal, CP 6128 Centre-Ville, Montréal, QC, Canada, H3C 3J7. E-mail: francois.peronnet{at}umontreal.ca.
ABSTRACT
Background:Glucose absorption from starchy food has only been described with small amounts ingested (2075 g).
Objective:Our aim was to describe total plasma (Ra) and exogenous glucose (Raexo) appearance, glucose release from the liver (HGP), and the metabolic response after ingestion of 5 g polished or parboiled rice/kg body mass.
Design:Gas exchange and urea excretion were monitored in 8 healthy subjects before (3.5 h) and after (8 h) ingestion of rice intrinsically labeled with 13C; [6,6-2H2]glucose was infused for the measurement of Ra, Raexo, and HGP.
Results:Changes in plasma glucose, insulin, lactate, and free fatty acids and the increase in Raexo and Ra (200%) and the decrease in HGP (90%) were not significantly different (P > 0.05) after ingestion of either rice. Glucose oxidation was not significantly different (111.6 ± 8.2 compared with 89.0 ± 11.3 g; P = 0.13), but fat oxidation was significantly lower (9.9 ± 1.7 compared with 21.3 ± 4.0 g; P < 0.05) after parboiled than after polished rice. The percentage of the glucose load that appeared in the circulation over 8 h was not significantly different after ingestion of polished (70.4 ± 4.5%) or parboiled (63.8 ± 2.0%) rice (P > 0.05).
Conclusion:Although the starch in parboiled rice is less susceptible to digestion in vitro, exogenous glucose availability was not significantly different after ingestion of large amounts of polished or parboiled rice. Glucose absorption remains incomplete 8 h after ingestion of both types of rice.
Key Words: Starch glucose kinetics stable isotope indirect respiratory calorimetry de novo lipogenesis insulin healthy men
INTRODUCTION
The consumption of starch, which is encouraged in a healthy diet (1), ranges between 140 and 390 g/d (2). However, exogenous glucose appearance in the peripheral blood (Raexo) from starchy food in humans has only been described with small amounts ingested (2075 g) (35). This is partly because U 13C-starch is not readily available. The 13C:12C in starch derived from plants naturally enriched in 13C is only 1.5% above the background 13C enrichment (6). Higher enrichments can only be obtained by growing starch-producing plants such as wheat (3, 4, 7) or leguminosa (5) in an atmosphere artificially enriched in 13CO2 (intrinsic labeling).
In the present experiment, Raexo and the metabolic response were described over 8 h after a starch meal in the form of rice (5 g dry mass/kg body mass) intrinsically labeled with 13C in young healthy male subjects, and plasma glucose kinetics and hepatic glucose output (HGP) were measured with use of [6,6-2H2] glucose infusion. Rice can be processed and cooked in various ways, which modify its physicochemical properties and the digestibility of the starch (810) and, in turn, could modify the glycemic index (8, 11). For example, consistent data indicate that the susceptibility of starch to digestion in vitro is lower in parboiled than in polished rice (810). As for the glycemic index, no significant difference was observed between these 2 types of rice by Larsen et al (12) and Miller et al (13). However, data reported by Casiraghi et al (8) and data compiled by Wolever (11) indicate that the glycemic index (compared with white bread) could be 2540% lower for parboiled [70 compared with 120 (8)] than for polished rice [51 compared with 68 (11)]. We, thus, compared Raexo, plasma glucose kinetics, and the metabolic response to ingestion of polished or parboiled rice intrinsically labeled with 13C. It was hypothesized that Raexo, along with the response of plasma glucose and insulin concentration, plasma glucose turnover, and the reduction in liver glucose production, would be lower after ingestion of the parboiled than polished rice.
SUBJECTS AND METHODS
Subjects
The experiment was conducted in 8 healthy active male subjects [age: 22.4 ± 0.6 y; weight: 68.0 ± 0.9 kg; height: 175.7 ± 1.3 cm; body mass index (BMI; in kg/m2) = 22.1 ± 0.6;
The subjects were studied 3.5 h before and 8 h after ingestion of 5 g (dry mass)/kg body mass of polished or parboiled rice intrinsically enriched in 13C. The rice was boiled for 14 (parboiled) or 12 min (polished) in tap water (1000 mL/125 g) with 5 g table salt/L water. The protocol followed a crossover design, and the order of presentation of the 2 types of rice was randomized. For 2 d before each experiment, the subjects were asked to rest and were provided with prepackaged meals (125 kJ · kg1 · d1: 20% proteins, 45% carbohydrates, 35% fat).
The subjects reported to the laboratory at 0730 after an overnight fast. After voiding and being weighed, the subject laid quietly for 30 min, and venous catheters (Adsyte 20GA; Becton Dickinson, Grenoble, France) were inserted into the left (for infusion of the tracer) and right (for drawing blood samples) forearms. A first 7-mL sample of blood was then withdrawn for determination of background plasma glucose enrichment in 13C and 2H, and infusion of [6,6-2H2] glucose (99% enriched; Masstrace, Worcester, MA) was initiated (0.08 mg · kg1 · in1 after a priming dose of 8 mg/kg; Ivac 591 infusion pump; Alaris Medical Systems, San Diego). The solution of glucose infused was passed through a 0.22-µm Millipore filter (Millipore Co, Bedford, MA) and was pyrogen free. After a 3-h equilibration period, with the subjects resting in a semisupine position, oxygen consumption (
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TABLE 1. Substrates ingested as polished or parboiled rice1
Rice intrinsically labeled with 13C
The rice was prepared by the Centre Français du riz and France riz (Arles, France) according to standard industrial procedures (14) and was made from rice (Oriza sativa L. cv Ariète) artificially enriched in 13C. For this purpose, a small amount of rice was grown hydroponically in a confined atmosphere containing 350 ppm CO2 artificially enriched in 13C (13CO2/CO2 11%; Euriso-top, Saint-Aubin, France). The rice artificially labeled with 13C (108 g; final 13C/C values measured by mass spectrometry = 10.4%) was mixed with rice grown in the field (6000 g; 13C/C = 1.0828%) to achieve a final 13C/C value in the meals of 1.25% (actual value: 1.247%).
Indirect calorimetry
Total protein oxidation and the associated amount of energy provided were computed from urea excretion in urine, and
The total rate of appearance of glucose in plasma (Ra) at time t was computed with use of Steeles equation corrected for nonsteady state and modified for stable isotopes, in conjunction with a spline-fitting program for smoothing both tracer and tracee concentrations (17):
RESULTS
Plasma glucose, lactate, free fatty acid, and insulin concentrations were not significantly different after ingestion of the 2 types of rice (Figure 1). When the data from the experiments with the 2 types of rice were pooled at each time point, the analysis showed that plasma glucose and insulin concentrations significantly increased, whereas plasma free fatty acid concentration significantly decreased. A small but significant increase in plasma lactate concentration was also observed. Plasma glucose, insulin, free fatty acid, and lactate concentrations were back to control values, respectively, at 360, 240, 480, and 360 min after the end of the meal.
FIGURE 1.. Mean (±SEM) plasma glucose, insulin, free fatty acid (FFA), and lactate concentrations before and during the 8 h after ingestion of polished or parboiled rice (the meal was ingested between 60 and 0 min). n = 8. No significant difference was seen between the 2 types of rice for any of the variables (two-factor repeated-measures ANOVA: main effect of type of rice, P > 0.05). *Line identifies the range of times significantly different from the premeal value (pooled data: one-factor repeated-measures ANOVA and Tukeys post hoc test, P < 0.05).
The oxidation rate of proteins was not significantly different before and after ingestion of polished (4.3 ± 0.4 g/h before the meal, providing 25 ± 2% of the energy yield; 3.6 ± 0.2 g/h after the meal, providing 19.8 ± 2.0% of the energy yield) or parboiled rice (3.2 ± 0.4 g/h before the meal, providing 22 ± 3% of the energy yield; 3.3 ± 0.3 g/h after the meal, providing 20.0 ± 2.1% of the energy yield) (two-factor analysis of variance for repeated measures; P > 0.05).
The significant changes in NPRQ after the meal (Figure 2) indicated a marked increase in glucose oxidation and a marked reduction in fat oxidation. However, over the 8 h after the meal, NPRQ only transiently increased above 1.0 (240 min after ingestion of parboiled rice); thus, no net de novo lipogenesis was present. The NPRQ values observed were significantly higher after ingestion of parboiled rice than polished rice (main effect of type of rice, without type of rice x time interaction). As shown in Table 2, the amount of fat oxidized was significantly lower after ingestion of parboiled rice than polished rice (main effect of type of rice, without effect of time and type of rice x time interaction). Glucose oxidation significantly diminished from 0240 to 240480 min (main effect of time, without effect of time and type of rice x time interaction) but was not significantly different after ingestion of parboiled or polished rice (P = 0.13).
FIGURE 2.. Mean (±SEM) respiratory exchange ratios corrected for protein oxidation [nonprotein respiratory quotient (NPRQ)] before and during the 8 h after ingestion of polished or parboiled rice (the meal was ingested between 60 and 0 min). n = 8. NPRQ was significantly higher after ingestion of parboiled than polished rice (two-factor repeated-measures ANOVA: main effect of type of rice without type of rice x time interaction, P < 0.05). *Line identifies the range of times significantly different from the premeal value (pooled data: one-factor repeated-measures ANOVA and Tukeys post hoc test, P < 0.05).
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TABLE 2. Glucose and fat oxidation after the rice meals1
Changes in tracer:tracee (x 100) for [6,6-2H2] and 13C-glucose from 60 to 480 min are shown in Figure 3. The 13C-glucose:glucose in plasma markedly increased after the meal and leveled off between 120 min and the end of the observation period, with 85% of plasma glucose deriving from ingested starch with both polished and parboiled rice. In response to the meal, both plasma glucose Ra and Raexo increased, whereas HGP significantly decreased and reached low values at the end of the observation period (Figure 4). No significant difference was observed between the kinetics of Ra, Raexo, and HGP after ingestion of the parboiled or polished rice. As shown in Table 3, the cumulative amounts of glucose, exogenous glucose, and glucose released from the liver appearing in the peripheral circulation were significantly lower between 240480 min than between 0240 min. However, no significant difference was observed after ingestion of parboiled or polished rice for any of these 3 variables. At the end of the observation period, the percentages of the glucose load which had appeared in the peripheral blood after ingestion of polished or parboiled rice were not significantly different (70.4 ± 4.5% and 63.8 ± 2.0%; paired t test, P > 0.05). No significant difference was observed between the cumulative amount of glucose that appeared in the circulation and the cumulative amount of glucose released from the liver after ingestion of the 2 types of rice.
FIGURE 3.. Mean (±SEM) plasma glucose enrichment in 13C and 2H (tracer:tracee x 100) before and during the 8 h after ingestion of polished or parboiled rice (the meal was ingested between 60 and 0 min). n = 8.
FIGURE 4.. Mean (±SEM) rates of appearance of plasma (Ra) and exogenous (Raexo) glucose into the peripheral circulation and hepatic glucose output (HGP) before and during the 8 h after ingestion of polished or parboiled rice (the meal was ingested between 60 and 0 min). n = 8. The y axes for each of the 3 panels is different. No significant difference was seen between the 2 types of rice for any of the variables (two-factor repeated-measures ANOVA: main effect of type of rice, without type of rice x time interaction, P > 0.05). *Line identifies the range of times significantly different from the premeal value (pooled data: one-factor repeated-measures ANOVA and Tukeys post hoc test, P < 0.05).
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TABLE 3. Cumulative amounts of glucose, exogenous glucose, and glucose released from the liver that appeared in the peripheral circulation after the rice meal1
DISCUSSION
Although consistent data indicate that starch in parboiled rice is less susceptible to digestion than starch in polished rice (810), Raexo and the percentages of glucose derived from the ingested starch which appeared into the peripheral circulation over the 8 h after the meal were not significantly different after ingestion of the 2 types of rice. In addition, except for a lower oxidation of fat with parboiled than polished rice, the metabolic responses did not differ markedly: changes in plasma glucose, insulin, lactate, and free fatty acid concentrations and the increase in Ra and the reduction in HGP were not significantly different after ingestion of the 2 types of rice.
Data from the present study about Raexo after ingestion of a large amount of rice in men (4.0 g/kg starch) compare well with those reported by Noah et al (20) in pigs with ingestion of 4.3 g/kg corn starch: peak Raexo and the percentage of glucose from the starch load that appeared into the peripheral circulation over 8 h (79 mg · kg1 · min1 and 6470%) were only slightly lower than those reported by Noah et al (20) (11 mg · kg1 · min1 and 73%). When 2075 g glucose [reviewed in Livesey et al (17)] or starch (35) are ingested in humans, peak Raexo only ranges between 3 and 7 mg · kg1 · min1, and 100% of exogenous glucose could appear into the peripheral circulation within 4-5 h after the meal. Thus, unlike the absorption of glucose from a small glucose or starch meal, the absorption of exogenous glucose from a large starch meal is not complete after 8 h, despite the much larger rate of appearance into the peripheral circulation.
As already discussed (21, 22) this could be due to several reasons. First, as indicated by the negative arterioportal gradient of 13C-glucose reported in pigs by Noah et al (20) 12 h after the end of the meal, glucose could still be absorbed from the gut at the end of the observation period. Second, a portion of exogenous glucose entering the portal vein could be taken up by the liver on first pass. Although this portion remains a matter of debate (2123), it could be as high as 30% (22, 23). It is worth mentioning that this percentage is close to the percentage of exogenous glucose that did not appear into the peripheral circulation in the present experiment (30% with polished rice and 36% with parboiled rice). Finally, a portion of exogenous glucose could be converted into 3-carbon products by the gut. For example, Abumrad et al (21) showed that 11% of a 1.63 g/kg glucose load actually enters the blood in the form of lactate and alanine.
Starchy food, including rice, can be processed and cooked in various ways that could modify their digestibility (810, 24), but a paucity of data exists about the actual effect of starch processing on Raexo (20) and on the metabolic response after a meal (25). In the study by Noah et al (20) pregelatinized starch was much more susceptible than native starch to hydrolysis in vitro (71% converted into maltodextrins within 180 min by -amylase, compared with only 22% for native starch). However, when compared with the native starch, peak Raexo was only 8% higher when the pregelatinized starch was ingested, and the amount of glucose that appeared into the peripheral circulation over the first 4 h after the meal was only 4% higher. Over the subsequent 4 h, the cumulative appearance of exogenous glucose into the peripheral circulation was actually 21% higher from the native than pregelatinized starch. In the present experiment, the susceptibility of the starch in the 2 types of rice was not measured, but consistent data from Casiraghi et al (8), Niba (9), and Rashmi and Urooj (10) indicate that starch from parboiled rice is less digestible than starch from polished rice. However, Raexo and the cumulative amount of exogenous glucose appearing into the peripheral circulation were not significantly different after ingestion of polished or parboiled rice (Figure 4 and Table 3). These observations and those from the study by Noah et al (20) suggest that the susceptibility of starch to hydrolysis might not be the rate-limiting factor for Raexo after ingestion of large starch meals. In this situation, the limiting factor could rather be the rate of glucose absorption by the gut.
This phenomenon could explain that, in the present experiment, changes in plasma glucose and insulin concentrations in response to the meal and changes in HGP were not significantly different after ingestion of polished or parboiled rice. Immediately at the end of the meal, plasma glucose and insulin concentrations were markedly increased but were not significantly different. As for HGP, it progressively decreased over the observation period, which is in line with data from several studies (3, 5, 17, 2123) after administration of small glucose or starch loads (3075 g), as well with data from Noah et al (20) after ingestion of a large amount of starch in pigs. However, the reduction was not significantly different after ingestion of polished or parboiled rice. In addition, despite the large value of Raexo and the elevated concentration of insulin, HGP was not totally suppressed. In fact, changes in HGP did not follow changes in plasma insulin or glucose concentrations. For example, HGP remained high over the first 4 h after the meal, at a time when plasma glucose and insulin concentrations were both high but decreased over the last 4 h of the observation period, when both plasma glucose and insulin concentrations decreased. Data from Noah et al (20) also indicate that HGP remained low (20% of premeal values) late in the observation period, although plasma insulin concentration was back to premeal values.
In the present experiment, in accordance with consistent data from several studies of disposal of a large carbohydrate load, fat oxidation was markedly reduced, whereas glucose oxidation was stimulated (7, 2629). However, changes in glucose compared with fat oxidation did not closely follow those in Raexo: although Raexo was not significantly different after ingestion of the 2 types of rice, fat oxidation was significantly lower after ingestion of parboiled than polished rice A possible explanation for these differences is that a portion of exogenous glucose could be oxidized in the gut, could be absorbed under the form of 3-carbon products, or both, as shown by Abumrad et al (21). This portion, which could be different after ingestion of parboiled or polished rice, escapes detection by the tracer techniques used in the present experiment, which only track the appearance of glucose in the peripheral blood.
ACKNOWLEDGMENTS
We are indebted to Martine Laville and her colleagues from the Centre de Recherche en Nutrition Humaine, Faculté de Médecine RTH Laennec, Lyon, for the measurement of 13C/12C in plasma glucose.
FP, XL, and MP initiated the study and developed the protocol and experimental design. The rice intrinsically labeled with 13C was grown under the supervision of MP. The experiments were performed by MK-A, DB, and HR. Data were compiled and analyzed by MK-A, HR, and FP and discussed with all of the authors. FP wrote the manuscript with contributions from MK-A, HR, and XL. None of the authors had any personal or financial conflicts of interest with regard to the study.
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