1 Institut National de la Recherche Agronomique, 44316 Nantes; and 2 Centre de Recherches en Nutrition Humaine, Groupe Métabolisme, 44035 Nantes, France
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ABSTRACT |
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Changes in
splanchnic metabolism in pigs were assessed after meals containing
slowly or rapidly digested starch. The pigs were fed a mixed meal
containing a "slow" native (n = 5) or a "rapid"
pregelatinized (n = 5) cornstarch naturally enriched with [13C]glucose. Absorption of
[13C]glucose was monitored by the arteriovenous
difference technique, and infusion of
D-[6,6-2H2]glucose in
the jugular vein was used to calculate the systemic appearance of
[13C]glucose. Arteriovenous balance data
obtained during a 12-h study period showed that the fraction of
ingested glucose equivalent appearing as glucose in the portal vein was
49.7 ± 7.2% for the slow starch and 48.2 ± 7.5% for
the rapid starch (P = 0.86). These values, corrected for the
gut extraction of circulating [13C]glucose,
became 66.4 ± 5.6 and 65.3 ± 5.6%, respectively (P = 0.35). Isotope dilution data indicated that systemic appearance of
exogenous [13C]glucose represented 62.9 ± 7.6 and 67.4 ± 3.0% of the oral load for slow and rapid
starch, respectively (P = 0.68). Arterial glucose utilization
by the gut increased from 7.3 ± 0.9 µmol · kg1 · min
1
before the meal to 8.5 ± 1.6 µmol · kg
1 · min
1
during absorption, independently of the nature of the starch. Thus
splanchnic glucose metabolism was unaffected by the nature of starch ingested.
starch; glucose metabolism; stable isotope
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INTRODUCTION |
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THE RATE OF ABSORPTION is probably a key factor in
splanchnic metabolism, because it regulates insulin secretion or action (20, 27). Although long-term consumption of slowly digested starches
can prevent the development of insulin resistance (12, 20, 27) and
obesity (15, 27) in rats, the postprandial effects of starch ingestion
on splanchnic glucose metabolism are not clearly known. This is
especially true when starch is ingested with other food products, which
can affect its bioavailability. Most studies in animal models have been
performed with glucose, and data have usually been obtained by the
arteriovenous balance technique. The isotope dilution method (dual
tracer approach), which has been frequently used in humans, can provide
further information on splanchnic metabolism. Isotope dilution, which is a noninvasive method, has shown that postprandial splanchnic metabolism is characterized by exogenous glucose retention (30% of
the ingested load) and suppression of endogenous glucose production (
80% of basal production) (9, 13, 16, 23). Although the use of both
arteriovenous balance and isotope dilution techniques can provide much
information about splanchnic metabolism, comparisons have rarely been
made between the data obtained from the two techniques. The aim of the
present study was to evaluate the impact of the bioavailability of
starch on splanchnic metabolism. For that purpose, pigs were given two
fully digestible cornstarches naturally enriched with
[13C]glucose, characterized as rapidly
(pregelatinized) or slowly (native) digestible starch. The two
complementary techniques of arteriovenous balance across the gut and
isotope dilution were used to assess the changes in splanchnic
metabolism after the meals.
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METHODS |
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Animals and Surgery
Studies were conducted on six conscious 24-h-fasted female Large White pigs, weighing 40-48 kg (mean: 43.7 ± 1.4 kg) at the time of the experiment. The animals were purchased from the Institut National de la Recherche Agronomique (INRA) Research Centre of Saint Gilles, France.Approximately 1-2 wk before the study, the animals underwent general anesthesia (O2, N2O, halothane). They were fitted with polyvinyl catheters (Tygon Norton, Cleveland, OH) in the jugular vein (1.6 mm ID, 3.2 mm OD), portal vein, and carotid artery (1.3 mm ID, 2.3 mm OD), and a flow probe (T206; Transonic Systems, Ithaca, NY) was positioned around the portal vein according to the technique previously described by Rérat et al. (24). The animals were allowed a minimum of 7 days for recovery after surgery. The experiment did not begin until they had recovered normal dietary intake and normal stools. The pigs were kept at room temperature in individual cages and were fed twice a day (9 AM and 4 PM) with the preexperimental diet. Animal treatment was always in accordance with French legislation.
Diets
Starches. The two purified cornstarches used in this study were supplied by Roquette Industries (Lestrem, France). These native ("standard", slowly digestible) and pregelatinized ("Pregeflo M," rapidly digestible) starches are totally digestible in the small intestine. Two pigs were fitted with an ileal cannula by the technique of van Leeuwen et al. (31) to obtain ileal effluents for starch measurements. The fraction of ingested starch entering the colon of these animals during the first 12 h after a meal was, respectively, 0.65 and 0.73% for pregelatinized starch and 0.46 and 0.30% for native starch. Only 2.8% (pregelatinized starch) and 0.8% (native starch) of the oral load still remained within the gut lumen after the pigs were killed at 12 h. The amounts of available glucose equivalent supplied by the two products were 207.7 g (native starch) and 198.0 g (pregelatinized starch).
Although both starches were highly digestible, the susceptibility of starch to hydrolysis was greater for pregelatinized than for native starch, as measured by the method of Bornet et al. (3). After 30 and 180 min of incubation withExperimental meals.
Two experimental meals providing 5,720 kJ (31% from lipids, 16% from
proteins, and 53% from carbohydrates) were given to the pigs (Table
1). The mixed meals contained either
"slow" native or "rapid" pregelatinized starch.
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Experimental Design
Each pig received the two experimental meals in randomized order, with an interval of 1 wk between experiments. Two pigs got only one of the two experimental meals. A total of 10 experiments was performed for the entire protocol (5 for the slow starch meal and 5 for the rapid starch meal). One week before the study, the pigs were fed a meal without naturally 13C-enriched foods (Table 1). At 7 AM on the day of the experiment (t =Blood samples (5 ml) were taken every 15 min during the first 4 h
(t = 120 min to t = 120 min), every 30 min
during the next 3 h (t = 120 min to t = 300 min), and
then every hour until the end of the study (t = 300 min to
t = 720 min). Blood was collected in heparinized tubes (Terumo,
Leuven, Belgium) and centrifuged (9,000 g for 10 min at
4°C). Plasma was isolated and kept at
20°C until analyzed.
Analytical Procedures
13C enrichment of starch. The 13C enrichment of glucose from starch was determined by the gas chromatography-combustion-isotope ratio mass spectrometry (GC-C-IRMS) method described by Tissot et al. (29). Native and pregelatinized starches were first hydrolyzed into glucose by use of a method modified by Thivend et al. (28). Five hundred milligrams of starch, mixed with 25 ml of distilled water, were heated at 100°C for 30 min. Then 2.5 ml of acetate buffer (pH = 4.6) were added, and the solution was completed with 45 ml of distilled water. Ten milligrams of amyloglucosidase (thermostable, Merck-Clévenot, Nogent-sur-Marne, France, cat. no. 1.01332, 2217 nKat/mg glucose equivalent) were added. Hydrolysis was stopped after 2 h of incubation by heating the solution at 100°C for 10 min. The hydrolysis products were then extracted by adding 188 ml of pure ethanol and mixing and centrifuging at 1,500 g (10 min). Supernatant was isolated and evaporated under vacuum. Glucose was then derivatized to glucose pentaacetate (21). The derivatized product was diluted in 1 ml of ethyl acetate (Sigma-Aldrich Chimie), and a sample (1 µl) was injected into a gas chromatograph (capillary column 30 m × 0.32 mm × 0.25 µm, type DB1, JW Scientific, Courtaboeuf, France). The gas chromatograph was coupled to a combustion furnace (CuO, NiO, Pt, 940°C), and an isotope ratio mass spectrometer (Delta S, Finnigan Mat, Bremen, Germany). Isotopomeric ions of CO2 were separated and recorded according to their mass-to-charge ratio (m/z) (44, 45, or 46). A standard CO2 sample of known enrichment was injected intermittently to ensure the high precision of measurements.
Plasma variables. Plasma glucose was measured by the glucose-oxidase method (Glucose Analyzer II, Beckman, Fullerton, CA). Insulin was measured by radioimmunoassay (ORIS, Gif sur Yvette, France). Plasma lactate was analyzed using an enzymatic test kit (Boehringer Mannheim, Meylan, France, cat. no. 139084).
Plasma [2H2]glucose and [13C]glucose isotopic enrichment. Fifty microliters of plasma were deproteinized by addition of 300 µl acetone. After 10 min at 4°C, the tube was centrifuged for 10 min at 4,000 g, and the supernatant was isolated. The supernatant was then evaporated under nitrogen, and the sample was derivatized.
13C plasma glucose enrichment (Calculations
Net [13C]glucose and lactate balance across
the gut.
Net gut balance (NGB) was calculated according to the formula described
by Rérat et al. (24)
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(1) |
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(2) |
Rate of glucose appearance in the systemic pool. The isotopic abundance of the samples was expressed in 13C atom % (AP). The AP of ingested and plasma glucose was transformed into atom % excess (APE) by the following formula: APE = APs-APb, where APs is the AP of the plasma sample, and APb is the AP of plasma glucose before the meal.
The rate of glucose appearance (RaT, mol · kg
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(3) |
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(4) |
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(5) |
Statistical Analysis
Statistical analyses involved standard error of the mean (SE), the Mann-Whitney test to compare the mean enrichments of native and pregelatinized cornstarch, and two-way analysis of variance to determine the effects of animals and test meals on metabolic variables. Analyses were performed using the Statgraphics 3.0 software package (STSC, Rockville, MD). ![]() |
RESULTS |
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13C Enrichment of Starch
After the starches were enzymatically hydrolyzed, no difference was observed between the 13C enrichments of derivatized glucose from slow or rapid starch (P = 0.87). The mean 13C enrichment of derivatized glucose was 1.0753 ± 0.0001 (n = 12) atom % 13C (AP).Absorption and Gut Metabolism (Arteriovenous Difference Technique)
Portal blood flow.
Basal portal blood flows were 21.25 ± 1.05 ml · kg1 · min
1
(n = 5) and 21.07 ± 0.65 (n = 5)
ml · kg
1 · min
1,respectively,
for slow starch and rapid starch meals (P = 0.36). Portal flows
increased to a mean of 31.43 ± 2.01 ml · kg
1 · min
1
at 45 min (slow starch) and 30.57 ± 2.18 ml · kg
1 · min
1
at 90 min (rapid starch) during the postprandial period, and they
returned to the basal level after 420 min. There was no difference between average portal flows measured after meals (25.21 ± 1.59 and
25.50 ± 1.17 ml · kg
1 · min
1
for slow and rapid starch, respectively; P = 0.55).
Glucose.
Basal arterial plasma glucose concentration was not different between
the slow starch meals (4.71 ± 0.14 mmol/l; n = 5) and the
rapid starch meals (4.55 ± 0.19 mmol/l; n = 5) (P = 0.30). Mean gut fractional extraction of glucose during the study was 7.6 ± 1.4 and 7.7 ± 2.5%, respectively, for slow starch and rapid starch meals (P = 0.16). The fraction of arterial glucose
extracted by the gut decreased after the meal and was minimal at 30 min for slow starch and at 90 min for rapid starch (Fig.
1). In basal state, the mean rate of
arterial glucose utilization by the gut was 6.6 ± 1.3 µmol · kg1 · min
1
for slow starch and 7.5 ± 1.4 µmol · kg
1 · min
1
for rapid starch (P = 0.91) (mean for both starches was 7.3 ± 0.9 µmol · kg
1 · min
1).
Under the meal fed condition, this rate was 8.8 ± 1.3 and 8.3 ± 3.2 µmol · kg
1 · min
1,
respectively, for slow and rapid starch (P = 0.20) (mean for both starches was 8.5 ± 1.6 µmol · kg
1 · min
1).
During absorption, the total amount of arterial glucose extracted was
57.4 ± 11.3 g for slow starch and 51.3 ± 20.0 g for rapid starch
(P = 0.20).
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Insulin.
Arterial plasma insulin concentration was 34.3 ± 7.3 pmol/l
(n = 5) and 37.1 ± 13.8 pmol/l (n = 5) before the
slow starch and rapid starch meals (P = 0.99). Maximal
increment over basal state, obtained 30 min after the beginning of the
meal (Fig. 4), was 216.4 ± 46.8 and 247.5 ± 41.7 pmol/l, respectively (P = 0.77). No
difference was observed between the two meals for the area under the
postprandial curve of insulin (P = 0.88).
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Lactate.
Mean arterial lactate concentration was 0.62 ± 0.08 mmol/l (n = 5) and 0.65 ± 0.09 mmol/l (n = 5), respectively, before the slow starch and rapid starch meals (P = 0.83). Net production of lactate by the gut occurred during the absorption period, and the
rate of production at maximum level (30 min) was not significantly different (P = 0.10) between the two meals (13.0 ± 1.3 µmol · kg1 · min
1
for slow starch and 13.0 ± 1.2 µmol · kg
1 · min
1
for rapid starch; n = 5). The total production of lactate by the gut amounted to 7.3 ± 1.4 g (3.5 ± 0.7% of the glucose
equivalent ingested; n = 5) and 6.7 ± 0.7 g (3.3 ± 0.3% of
the glucose equivalent ingested; n = 5) for slow starch and
rapid starch meals, respectively (difference not statistically
significant, P = 0.35).
Isotope Dilution Data
Rate of systemic appearance of glucose.
The rate of total glucose appearance (RaT) was 17.23 ± 1.18 and 13.92 ± 1.11 µmol · kg1 · min
1,
respectively, before the slow starch meal (n = 5) and the rapid starch meal (n = 5) (P = 0.10). Glucose production
increased to maximal values at 90 min for slow starch (70.25 ± 9.08 µmol · kg
1 · min
1)
and at 75 min for rapid starch (61.35 ± 3.49 µmol · kg
1 · min
1)(P = 0.45).
Systemic appearance of endogenous and exogenous glucose.
During absorption, endogenous glucose production was suppressed an
average of 59.9 ± 8.3% (n = 5) after the slow starch meal and 69.7 ± 5.7% (n = 5) after the rapid starch meal (Table
2), corresponding to equivalent amounts of
glucose retained in the splanchnic bed of 59.0 ± 10.2 g and 54.8 ± 6.5 g, respectively (P = 0.55) (Fig.
5).
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Comparison of arteriovenous difference and isotope dilution data.
The cumulated amounts of [13C]glucose appearing
in the portal vein (calculated using the net balance across the gut, or
the net balance corrected for the extraction of circulating
[13C]glucose) and the cumulated amounts of
[13C]glucose appearing in systemic blood
(calculated using the isotope dilution method) were determined for slow
and rapid starches (Fig. 6). With either
test meal, the values calculated by the different methods were similar
during the first 240 min of the study. Then, values obtained by the
arteriovenous difference method, uncorrected for the extraction of
circulating [13C]glucose, became lower than the
values calculated by the isotope dilution method. For both meals, the
cumulated amounts of glucose determined by the isotope dilution
technique at 720 min were 25% higher than those obtained with the
arteriovenous difference method. Values were significantly different
between the two methods at 600 min, 660 min, and 720 min only for the
rapid starch meal (P < 0.05). When corrected for the
extraction of circulating [13C]glucose, the
values calculated by the arteriovenous difference method were similar
to those determined by isotope dilution.
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DISCUSSION |
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Splanchnic metabolism of glucose from a slowly or rapidly digested
starch was considered in this study. The pig, because of its
physiological similarities with humans, was used as the animal model
(18). Splanchnic glucose metabolism was assessed simultaneously with
the arteriovenous difference technique (to measure net glucose absorption) and the isotope dilution (dual tracer) technique, after the
pigs had received isocaloric (5,720 kJ) meals containing 53% of
their energy intake as starch.
A low average blood flow rate was found after the test meals (25.5
ml · kg
1 · min
1)
compared with the range of values reported for pigs (24-40
ml · kg
1 · min
1)
(2, 8, 24). However, because the transit time ultrasound method has
been validated in vivo (7), measurements may depend on the amount and
type of diet rather than on the technique used. Moreover, no
development of collateral circulation in the portal system was observed
when pigs were autopsied at the end of each experiment.
In basal state, the rate of glucose utilization by the gut was 7.3
µmol · kg
1 · min
1.
During absorption, the gut switched from net glucose utilization to net
glucose release. However, it is remarkable that glucose utilization by
the gut increased substantially in the meal fed condition. The gut used
both luminal glucose from starch digestion, and vascular glucose, whose
rate of utilization increased during absorption. The extraction ratio
of vascular glucose decreased between 30 and 90 min after the meals,
but arterial glucose was still partially extracted by the gut during
absorption, mainly in the latest phase of this absorption (after the
first 240 min of the study). For both starches, the rate of utilization
increased during absorption. Abumrad et al. (1) showed that glucose
utilization by the gut is increased during absorption. Although
Vaugelade et al. (32) observed a decreased glucose oxidation capacity of enterocytes in postprandial conditions (in the presence of glutamine), they reported a high glycolytic capacity for the intestinal muscular layer, which may have contributed to the metabolism of both
endogenous glucose and [13C]glucose (from
starch digestion) in our study.
Absorption of [13C]glucose tended to be higher
during the first 105 min after the rapid starch meal. The pig has high
digestive capacities (18), which may explain why the difference in the rates of glucose absorption for the two starches was not as large as
expected from in vitro results. The proportion of ingested [13C]glucose equivalent that appeared in the
portal vein was low (50%) for both test meals. However, when the
values were corrected for recycled [13C]glucose
uptake by the intestine, the proportion of ingested [13C]glucose equivalent entering the portal
vein (
65% for both meals) was more in accordance with the
70-80% generally measured after a pure glucose load (1, 2). On
the basis of these last data, the gut would have retained
35% of
the dietary glucose load (
70 g) during the postprandial study
period. However, this proportion is overestimated, because absorption
was not fully ended 12 h after the meals. Indeed, the rates of
[13C]glucose portal flux were still 6.5 ± 4.6 µmol · kg
1 · min
1(slow
starch) and 6.0 ± 1.9 µmol · kg
1 · min
1(rapid
starch) at the end of our experimental period.
Part of the ingested starch was metabolized by the gut into lactate.
After both test meals, lactate production by the gut (7 g) accounted
for 3.5% of the ingested glucose equivalent, which is in agreement
with values found in different species (1, 24, 30). Only minor gut
production of alanine (3-5% of the glucose equivalent ingested)
has been reported after an oral glucose load (1) or a mixed meal (17).
Therefore, the fraction of the ingested glucose equivalent lacking in
the balance (
30%) must be related either to the conversion of
glucose into other metabolites (such as CO2, for example)
or to the uncompleted absorption at the end of the study. It is
unlikely that part of the starch was fermented in the gut, because
short-chain fatty acid concentration in ileal residues did not increase
during the experiment (studies in one pig; results not shown) and
little carbohydrate entered the colon in either animal (see
RESULTS).
Basal glucose production (14-17
µmol · kg1 · min
1)
was similar to that reported for pigs (10, 19) and slightly higher than the values of 8-13
µmol · kg
1 · min
1
observed for humans (9, 13, 16, 23, 29). In the present article, the
systemic appearance of glucose was calculated according to the
single-compartment model described by Steele (26), which has mainly
been used for glucose metabolism studies (22, 25, 29). This model does
not really describe the complex physiology of glucose metabolism but is
reliable at slow turnover rates (4). Moreover, although an error due to
the use of too low a glucose distribution volume (V = 0.2 l/kg) has
been found, it was shown to be partly counterbalanced by glucose
recycling (16). The systemic appearance of exogenous glucose was not
different for the two experimental meals. The similar cumulated amounts
of [13C]glucose calculated by the isotope
dilution and arteriovenous difference techniques during the first 240 min of the study suggest that hepatic fractional extraction of absorbed
glucose was low (9, 23). After 240 min for both test meals, the
cumulated amounts of [13C]glucose calculated by
the isotope dilution method were higher (
25% higher at 720 min)
than those calculated by the arteriovenous difference technique.
Glucose recycling, via gluconeogenesis (11), might account for part of
the discrepancy observed between stable isotope and arteriovenous
difference data. However, it has been shown after a pure glucose load
that the rate of glucose recycling is low during 240-360 min after
the oral load (13, 16). It was also suggested that exogenous glucose
(newly absorbed) may be taken up first by the liver and incorporated
into the glycogen pool before being released into the systemic
circulation at the end of the study period. Indeed, Moore et al. (17)
reported net hepatic release of absorbed
[13C]glucose tracer in dogs 300 min after the
ingestion of a mixed meal. Our findings do not support this hypothesis,
because at no period of the study were the arterial glucose
13C enrichments higher than the portal glucose
13C enrichments. Moreover, when the cumulated amounts of
[13C]glucose obtained by arteriovenous
difference were corrected for recycled
[13C]glucose uptake by the intestine, they were
similar to those calculated for isotope dilution. This suggests that
the difference between the two methods might only be related to the
extraction of recirculating exogenous glucose by the gut. Our findings
are consistent with an appropriate use of the isotope dilution method as an alternative approach to measure the rate of
[13C]glucose absorption.
In conclusion, the concomitant use of arteriovenous balance across the gut and isotope tracers showed that glucose utilization by the gut increased substantially during absorption and that this was unaffected by the nature of the starch ingested.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for correspondence and reprint requests: M. Champ, INRA, rue de la Géraudière, BP 71627, 44316 Nantes, Cedex 03, France (E-mail: champ{at}nantes.inra.fr).
Received 25 February 1999; accepted in final form 15 September 1999.
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