Download Absorption from different intestinal segments during exercise

Absorption from different intestinal segments
during exercise
G. P. LAMBERT, R. T. CHANG, T. XIA, R. W. SUMMERS, AND C. V. GISOLFI
Departments of Exercise Science and Internal Medicine,
University of Iowa, Iowa City, Iowa 52242-1111
duodenum; jejunum; fluid balance; fluid absorption; solute
absorption
of fluid homeostasis during prolonged exercise is the ability to absorb ingested fluids
(19), which occurs primarily in the proximal small
intestine (duodenojejunum). Segmental perfusion is
the most accepted technique for study of intestinal
absorption of different solutions (47); however, the
results only apply to the segment studied. Previous
investigations (1, 17, 21–23, 26, 29, 39, 41, 46, 54) have
differed in the site of perfusion (e.g., duodenojejunum,
jejunum, ileum), which has led to difficulty in comparing results and drawing conclusions regarding the
efficacy of various solutions. Furthermore, caution must
be exercised in applying the results of direct perfusion
studies to what would occur if the same solution were
orally ingested.
Recently, we developed a technique to simultaneously determine both gastric emptying (GE) and
AN IMPORTANT ASPECT
204
intestinal absorption (28). This technique allows determination of intestinal water and solute flux, while also
accounting for individual GE rates and alterations
made by the stomach to the solution after its oral
ingestion. This technique was employed in the present
investigation to determine whether different segments
of the proximal small intestine absorb water and
nutrients at different rates.
In humans, the duodenum is defined as the portion of
intestine from the pyloric sphincter to the ligament of
Treitz and is 20–30 cm in length (10, 33). It is highly
permeable and presumably the site of maximal fluid
movement between the alimentary canal and the blood.
It is often cited as the intestinal segment responsible
for bringing chyme from the stomach to isotonicity (51).
Most segmental perfusion studies bypass this segment
and typically evaluate jejunal function beyond the
ligament of Treitz. If the purpose of performing segmental perfusion in the jejunum is to evaluate the efficacy of
ingesting the same solution, such an extrapolation may
be inaccurate. In contrast to the duodenum, the jejunum consists of a less leaky mucosal epithelium with a
significantly greater ability to absorb glucose (24).
Results of a pilot study from this laboratory (Fig. 1)
indicate significantly greater fluid absorption with
ingestion of a water placebo (WP) compared with an
isotonic 6% carbohydrate-electrolyte (CHO-E) beverage
in the duodenum. This contrasts with previous findings
(22, 23) in which primarily the jejunum was studied by
the segmental perfusion technique. From these data,
we questioned whether segmental differences exist for
fluid and solute absorption.
Given the large osmotic gradient between water and
blood, we hypothesized that absorption of water would
be greater in the duodenum (first 25 cm) compared with
an isotonic solution. In the jejunum (second and third
25-cm segments), where membrane resistance is greater
than in the duodenum but where glucose transport is
enhanced (24), we hypothesized an isotonic CHO-E
beverage would have an absorptive advantage over
deionized water because of CHO absorption and subsequent ‘‘solution drag.’’ To test these hypotheses, we
studied water and solute absorption of two different
solutions (a deionized WP and an isotonic CHO-E
solution) in three consecutive segments of the proximal
small intestine (,0–25, 25–50, and 50–75 cm distal to
the pyloric sphincter).
MATERIALS AND METHODS
Six healthy men and one woman [age 26.0 6 9.0 yr; peak
oxygen consumption (V̇O2 peak) 5 53.5 6 6.5 ml · kg21 · min21]
participated in this study, which conformed to all the rules
and regulations of the University of Iowa Human Use Commit-
0161-7567/97 $5.00 Copyright r 1997 the American Physiological Society
http://www.jap.org
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Lambert, G. P., R. T. Chang, T. Xia, R. W. Summers,
and C. V. Gisolfi. Absorption from different intestinal segments during exercise. J. Appl. Physiol. 83(1): 204–212,
1997.—This study evaluated intestinal absorption from the
first 75 cm of the proximal small intestine during 85 min of
cycle exercise [63.6 6 0.7% peak O2 consumption (V̇O2 peak)]
while subjects ingested either an isotonic carbohydrateelectrolyte beverage (CHO-E) or a water placebo (WP). The
CHO-E beverage contained 117 mM (4%) sucrose, 111 mM
(2%) glucose, 18 meq Na1, and 3 meq K1. The two experiments were performed a week apart by seven subjects (6 men
and 1 woman; mean V̇O2 peak 5 53.5 6 6.5 ml · kg21 · min21 ).
Nasogastric and multilumen tubes were fluoroscopically positioned in the gastric antrum and duodenojejunum, respectively. Subjects ingested 23 ml/kg body weight of the test
solution, 20% (383 6 11 ml) of this volume 5 min before
exercise and 10% (191 6 5 ml) every 10 min thereafter. By
using the rate of gastric emptying (18.1 6 1.1 vs. 19.2 6 0.7
ml/min for WP and CHO-E, respectively) as the rate of
intestinal perfusion, intestinal absorption was determined by
segmental perfusion from the duodenum (0–25 cm) and
jejunum (25–50 and 50–75 cm). Water flux was different (P ,
0.05) between solutions in the 0- to 25- and 25- to 50-cm
segments for WP vs. CHO-E (30.7 6 2.7 vs. 15.0 6 2.9 and
3.8 6 1.1 vs. 11.9 6 3.3 ml · cm21 · h21, respectively). Furthermore, water flux differed (P , 0.05) for WP in a comparison of
the 0- to 25- to the 25- to 50-cm segment. Total solute flux
(TSF) was not significantly different among segments for a
given solution or between solutions for a given segment.
There was no difference between trials for percent change in
plasma volume. These results indicate that 1) fluid absorption in the proximal small intestine depends on the segment
studied and 2) solution composition can significantly effect
water absorption rate in different intestinal segments.
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ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
tee. Each subject gave signed informed consent and received a
physical examination before participation. V̇O2 peak was determined by using a graded protocol on an electronically braked
cycle ergometer (The Bike, Cybex, Ronkonkoma, NY). Expired gases and ventilation were analyzed with a Q-Plex I
metabolic system (Quinton Instruments, Seattle, WA). A
workload corresponding to 60–65% V̇O2 peak was subsequently
determined and served as the exercise intensity for the
experimental trials.
Subjects followed a controlled diet for 16–18 h before each
experiment and were asked to limit their physical activity
during this time to control preexperiment glycogen levels.
The morning of an experiment, the subject arrived at the
University of Iowa Hospitals and Clinics at ,5 AM after an
overnight fast (at least 8 h) and was orally intubated with a
nasogastric (NG) tube (50 in., 14 Fr, Levin) into the gastric
antrum and a multilumen tube (construction described below) into the duodenojejunum. During tube placement the
subject ingested water (,400–500 ml) to facilitate movement
of the tubes and to control for preexperiment hydration
status. The NG tube was attached to the multilumen tube
with a small piece of thin rubber tubing so that its distal tip
was 9 cm from the proximal sampling site of the multilumen
tube. The rubber tubing was located 7 cm from the distal tip of
the NG tube to allow the NG tube to separate from the
multilumen tube in the stomach without passing into the
duodenum. Tube placement was verified fluoroscopically, and
contrast medium [Hypaque sodium 50%; a brand of diatrizoate sodium injection (USP)] was injected through the
proximal sampling port during placement of the tube to
ensure that the tube was positioned correctly. When both
tubes were in position, the most proximal port of the multilumen tube was located ,5 cm from the pyloric sphincter, and
the NG tube was positioned in the distal antrum.
During positioning of the tubes, an 18-gauge, 13⁄4-in. catheter was placed in a superficial arm vein for blood sampling.
Determination of Stomach Volume, GE Rate,
and Gastric Secretion
Stomach volume was determined every 10 min by using a
modified version of the repeated double-sampling techniques
described by George (18) and modified by Beckers et al. (2).
Gastric secretion was calculated on the basis of the formula of
Murray et al. (35) in accordance with Beckers et al. (2).
Briefly, the procedure involves obtaining 5-ml gastric samples
and injecting 15 ml of PR (200 mg/l) every 10 min with a 70-ml
Toomey syringe. The technique is as follows: 1) a gastric
sample is obtained; 2) PR is injected, mixed thoroughly with
the stomach contents, and another sample is obtained; and 3)
the subject ingests the test solution, the new stomach contents are mixed, and a final sample is drawn. The samples
obtained in steps 1–3 are used to calculate stomach volume
and gastric secretion every 10 min as follows
Stomach volume (ml) 5 PRvol 3
PRinj 2 PRafter add
PRafter add 2 PRbefore add
where PRvol is volume of PR injected every 10 min, PRinj is the
concentration of PR injected, PRafter add is the concentration of
PR in the stomach contents after PR is added and mixed well,
and PRbefore add is the concentration of PR in the stomach
before PR injection.
Gastric secretion is calculated as
GS10 5 stomach volume 3 [1 2 (PR10 /PR0)]
where GS10 is the volume of gastric secretion in the stomach
contents after each 10-min period from the time a subject
drinks to the time stomach volume is determined 10 min
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Fig. 1. Individual data from a pilot study investigating water flux in
first 25 cm of small intestine comparing a water placebo (WP) to an
isotonic carbohydrate-electrolyte (CHO-E) beverage. Values are
means 6 SE. Arrows, 7 of 8 subjects exhibited higher rates with a WP
compared with CHO-E.
After tube placement, the subject walked to the exercise
physiology laboratory and sat for 20 min to allow plasma
volume to equilibrate. After 20 min, blood and urine samples
were collected, a rectal temperature (clinical thermometer),
resting heart rate (heart rate monitor; Polar Vantage XL,
Polar USA, Stamford, CT), and nude body weight were
obtained, and the subject changed into cycling clothes. The
subject then immediately mounted the stationary bike, and
stomach contents were aspirated through the NG tube.
After stomach aspiration, the subject drank an initial bolus
of test solution equaling 20% of the total volume ingested (23
ml/kg body wt). The total volume averaged 1,914 6 191 ml,
and the mean initial bolus was 383 6 37 ml. Five minutes
after ingestion, the subject began cycling for 85 min. Each
10-min interval thereafter, an additional amount of test
solution was ingested and equaled 10% of the total experimental volume (191 6 19 ml). The experimental solutions consisted of either a 117 mM (4%) sucrose, 111 mM (2%) glucose,
17.8 meq/l Na1, and 3.1 meq/l K1 beverage with an osmolality
of 282 mosmol/kgH2O (i.e., CHO-E), or a deionized WP
(osmolality 5 1.1 mosmol) flavored to match the CHO-E
solution. Each solution also contained 1 mg/ml polyethylene
glycol 3350 (PEG). The temperature of the solution, which
was given to the subject in a clear graduated flask, was
10–15°C. Experiments were performed in a 22°C environment with a slight breeze (,2 ft /s) produced by a fan placed in
front of the subject. Blood samples were drawn every 15 min
to determine changes in plasma volume, osmolality, Na1, K1,
and glucose. Heart rate was obtained every 15 min. Rectal
temperature, nude body weight, and urine volume were
recorded postexercise. Sweat rate was calculated from nude
body weight change pre- to postexperiment corrected for fluid
ingestion, phenol red (PR) injection, and stomach, intestinal,
blood, and urine samples.
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ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
later. Stomach volume is that determined for the 10-min
period under study, PR10 is the PR concentration in the
stomach before the stomach volume is determined (after 10
min have elapsed since drinking), and PR0 is the PR concentration in the stomach immediately after the initial drink (10
min before). GE rate is derived by subtracting a given
stomach volume from the volume that is in the stomach after
the previous ingestion of beverage 10 min before.
Determination of Intestinal Absorption
by Segmental Perfusion
Q̇E 5 GER · [PEG]s /[PEG]p 2 ṠP
Q̇L 5 Q̇E · [PEG]p /[PEG]d
Q̇N 5 Q̇L 2 Q̇E
where GER is the gastric emptying rate; Q̇E is the flow rate
entering a given segment (ml/min); Q̇L is flow rate leaving a
given segment (ml/min); Q̇N is the net water movement across
the wall of the segment of intestine studied (ml/min); ṠP is
sampling rate from proximal collecting sites for each segment
studied; and [PEG]s, [PEG]p, and [PEG]d are the concentrations of the nonabsorbable marker in the stomach, at the
proximal site of a given segment, and at the distal site of a
given segment, respectively. Individual segments along the
total 75-cm test length (i.e., 25–50 cm and 50–75 cm) were
calculated by subtraction after determination of flux in the 0to 25-, 0- to 50-, and 0- to 75-cm segments, respectively. Solute
flux was calculated by multiplying the solute concentration at
the proximal and distal sampling sites of the 0- to 25-, 0- to
50-, and 0- to 75-cm segments and by the flow rates entering
and leaving these segments. Net movement of solute in these
segments was determined by using the formulas of Cooper et
al. (3). Solute fluxes in individual segments (i.e., 25–50 cm
and 50–75 cm) were calculated in the same manner as
described above for water flux. In the making of these
calculations, negative values indicate absorption and positive
values, secretion. However, for ease in presenting the results,
the signs have been switched (positive values 5 absorption;
negative values 5 secretion). All results were calculated after
a 35-min equilibration period to allow a steady state to be
reached (3, 46). Samples were collected during the equilibration period but were not used in data analysis.
PR concentration in the stomach samples was measured
spectrophotometrically at 560 nm after dilution (0.3-ml sample in 5-ml deionized water) and alkalinization with 1 ml
borate buffer (pH 9.2) (18, 48). All samples and standards
were analyzed in duplicate, with deionized water serving as a
reference blank. PEG in the intestinal samples was determined by the method of Hyden (27) as modified by Malawer
and Powell (32). Osmolality was measured by using freezingpoint depression (Multi-Osmette, Precision Systems, Natick
MA), Na1 and K1 concentrations ([Na1] and [K1], respectively) by flame photometry (model IL 943, Instrumentation
Laboratory, Lexington MA), and CHO by high-performance
liquid chromatography (Dionex DX-500 System, Sunnyvale,
CA). Samples that contained sucrose were hydrolyzed with
8.75 N trifluoracetic acid before measurement to liberate
glucose and fructose. This allowed for a more accurate
determination of CHO flux in the intestine. Percent change in
plasma volume was calculated on the basis of the method of
Dill and Costill (13).
Statistical Analysis
Data were tested for normality by using the Shapiro-Wilk
test. The null hypothesis of the data, being a normal distribution, was not rejected (P . 0.05). A two-factor analysis of
variance (ANOVA) with repeated measures was then used to
determine 1) the effect of solution and intestinal segment on
water and solute flux, 2) the effect of solution and intestinal
segment on solution composition, 3) the effect of solution and
time on blood and solution composition measurements, and 4)
the effect of solution and time on PEG concentration at the
various sampling sites. One-factor ANOVA and one-factor
ANOVA with repeated measures were employed 1) when
significant P values (P , 0.05) were observed in the two-factor
ANOVA and 2) to compare mean values for sweat rate,
percent body weight loss, urine production, rectal temperature, and heart rate. The Fisher post hoc test was utilized to
identify significant differences (P , 0.05).
Fig. 2. Stomach volumes and gastric emptying rates at each 10-min
period during experiment after 35-min equilibration period. Values
are means 6 SE.
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The technique is described elsewhere (23), but changes
made to fit this protocol are as follows.
Multilumen tube specifications. The multilumen tube (Arndorfer, Greendale, WI) was 240 cm long and had five lumens,
each 2 mm in diameter. At the end of the tube, a latex balloon
was attached with 2–0 silk and held 1.5 ml of mercury
enclosed in a double bag of latex. One lumen served to inflate
the balloon, another to sample fluid from the proximal site of
the test segment (,5 cm past the pyloric sphincter), and other
lumens to sample fluid 25, 50, and 75 cm distal to the
proximal site. These were glued together in a semirounded
configuration. The sampling sites had three holes spaced 1 cm
apart located at the top and bottom of the lumen, with a
polyvinyl basket over one side to prevent the holes from
lodging in the intestinal mucosa.
During each 10-min interval of the experiment, intestinal
fluid was collected at a rate of 1 ml/min from the proximal,
25-cm, and 50-cm sampling sites, and by constant siphonage
at the 75-cm sampling site. Net water flux values were
calculated for each interval according to the following equations (3)
Analytical Procedures
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ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
Table 1. Comparisons of sweat rate, percent body weight loss, urine production, final rectal temperature,
and final heart rate between the 2 experimental conditions
Solution
Sweat Rate,
l/h
Body Wt Loss,
%
Urine
Produced, ml
Final Rectal
Temperature, °C
Final Heart Rate,
beats/min
WP
CHO-E
1.13 6 0.10
1.11 6 0.02
0.18 6 0.15
0.18 6 0.09
255 6 97
166 6 35
38.4 6 0.10
38.5 6 0.08
146 6 7
146 6 5
Values are means 6 SE; n 5 7 subjects. WP, water placebo; CHO-E, carbohydrate-electrolyte beverage.
The pilot study referred to at the beginning of this study
was carried out identically to the methods described above,
except that there was only a 0- to 25-cm test segment in the
multilumen tube (for specifics, see Ref. 27).
RESULTS
Fig. 3. Individual water flux data in segments of proximal small intestine. Mean
values are 6 SE. A: 0- to 25-cm segment.
Arrows, all 7 subjects exhibited higher
rates of water absorption with WP compared with CHO-E. B: 25- to 50-cm segment. Arrows, 6 of 7 subjects had greater
water absorption with CHO-E compared
with WP. C: 50- to 75-cm segment. No
significant difference was observed between beverages (arrows were not necessary). D: 0- to 75-cm segment. No significant difference was observed between
beverages (arrows were not necessary).
* Significantly different from WP, P , 0.05.
# Significantly different from 0–25 cm, P ,
0.05.
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All subjects began the experiments in a euhydrated
state on the basis of plasma osmolality values (290 6 1
mosmol/kgH2O for both WP and CHO-E). There were
no differences in cardiovascular, fluid, or thermoregulatory measurements (sweat rate, percent body weight
loss, urine production, rectal temperature, final heart
rate) between the two experimental conditions (Table 1).
Fluid ingestion offset fluid losses due to sweating and
sample collection (see %body weight loss, Table 1).
Mean GE did not differ between the two drinks
(18.1 6 1.1 vs. 19.2 6 0.7 ml/min for WP and CHO-E,
respectively). Mean gastric secretion rates were also
not different for the two solutions (26.0 6 7.1 vs. 23.7 6
10.8 ml/10 min for WP and CHO-E, respectively). GE
was maintained at a steady rate by producing a relatively constant stomach volume. There were no differences over time for stomach volume or GE in either
experiment after the 35-min equilibration period (mean
stomach volume postequilibration: WP 5 264 6 60 ml;
CHO-E 5 240 6 43 ml) (Fig. 2). In terms of intestinal
steady-state conditions (after the 35-min equilibration
period), no differences were observed in PEG concentrations at a given sampling site over time for a given
solution. However, significant differences were observed in mean fluid absorption in the different segments of the small intestine for a given solution (Fig. 3).
Moreover, water flux in specific areas of the small
intestine was dependent on solution composition (Fig. 3).
When the whole 75-cm segment was examined, no
difference occurred in water absorption (12.4 6 1.1 vs.
10.4 6 1.1 ml · cm21 · h21 for WP and CHO-E, respectively) (Fig. 3). Total water absorption for the whole
75-cm segment accounted for 83 and 72% (not sigificant) of the fluid available for absorption (after correction for fluid sampled from the stomach and intestine)
for WP and CHO-E, respectively. Of the fluid absorbed,
80 and 82% were retained for WP and CHO-E, respectively, when urine production (Table 1) was taken into
account. Total solute flux (TSF) was significantly different (0.8 6 0.2 vs. 4.2 6 0.3 mmol · cm21 · h21 for WP and
CHO-E, respectively; P , 0.05) over the entire 75 cm.
TSF did not differ among segments for a given solution,
or between beverages within segments, although the
CHO-E solution exhibited higher rates for TSF compared with WP (Fig. 4). The difference in TSF is
primarily attributable to CHO flux for the CHO-E
beverage (Table 2).
The osmolality of the WP increased significantly (P ,
0.05) at each sampling site in the intestine as it moved
distally (Fig. 5), which was reflected in [Na1] and [K1]
changes (Figs. 6 and 7). These changes were smaller
during the CHO-E trial, although significant increases
(P , 0.05) were observed for values for this solution in
the stomach and proximal sampling site compared with
sites 25 cm and beyond. Net fluxes for both Na1 and K1
are presented in Table 2.
Plasma volume was not significantly different between trials at any time point throughout the experiments (Fig. 8). Plasma osmolality increased significantly (P , 0.05) during exercise in both trials but did
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ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
not change after the 35-min equilibration period, and
there was no difference between experiments at any
time point except at 45 min, when the WP (292 6 2
mosmol/kgH2O) was significantly lower than CHO-E
(297 6 1 mosmol/kgH2O). Mean plasma osmolality
values for the postequilibration period were 293 6 2
and 295 6 1 mosmol/kgH2O for WP and CHO-E,
respectively. Plasma [Na1] did not change with exercise
time, and the values did not differ at any point between
beverages (mean values postequilibration 5 142.1 6
0.9 vs. 143.5 6 0.4 meq/l for WP and CHO-E, respectively). Plasma [K1] increased significantly at each
time point in both trials (P , 0.05), although no
differences were observed between trials at these times,
nor were the postequilibration mean values different
between trials (4.76 6 0.06 vs. 4.81 6 0.06 meq/l for WP
and CHO-E, respectively). Plasma glucose concentration was maintained throughout the exercise protocol
during ingestion of CHO-E but declined significantly
during the WP trial, resulting in significant differences
between the two trials for the final 55 min of the
experiment (mean values postequilibration 5 5.4 6
0.09 vs. 4.7 6 1.0 mM for CHO-E and WP, respectively).
DISCUSSION
This is the first study to simultaneously measure
intestinal absorption from sequential segments of the
proximal small intestine together with GE of beverages
consumed orally during exercise. The results provide
Fig. 5. Osmolality of ingested solutions in stomach and at various
sites in proximal small intestine. Values are means 6 SE. * Significantly different from WP. # Significantly different from stomach site,
P , 0.05. †Significantly different from 0-cm site, P , 0.05.
& Significantly different from 25-cm site, P , 0.05. @ Significantly
different from 50-cm site, P , 0.05.
evidence that fluid absorption from a given solution
varies from one segment to another and with the
composition of the ingested solution. The following
discussion focuses on 1) potential mechanisms to explain this differential segmental absorption (duodenal
vs. jejunal), 2) the consequences of bypassing the
duodenum in intestinal absorption studies, 3) gastric
influences, and 4) the relationship of intestinal absorption to fluid balance, thermoregulation, and energy
substrate availability. It is important to note that these
experiments were performed by euhydrated, healthy
subjects during cycle exercise at 60–65% V̇O2 peak.
Duodenal Absorption (0–25 cm)
The duodenum is considered the most permeable
portion of the small intestine to water, and its primary
function is to bring either hyper- or hypotonic chyme to
isotonicity through net secretion or absorption of water
and diffusable ions (51). The greater fluid absorption
observed in the duodenum during ingestion of the WP
compared with the CHO-E beverage is attributable to
the osmotic superiority of the WP and passive movement of water down its concentration gradient. The WP
entered the duodenum at an osmolality of 52 6 11
mosmol/kgH2O and had an osmolality of 164 6 12
Table 2. Na1, K 1, and CHO fluxes in intestinal segments studied
Na1 Flux
K1 Flux
CHO Flux
Intestinal
Segment
WP
CHO-E
WP
CHO-E
0–25-cm
25–50-cm
50–75-cm
0.0160.47
0.1960.44
1.9960.65†
21.0460.36
1.2260.33†
1.8760.10†
0.0960.02
0.0360.01
0.0560.01
0.060.03
0.1260.03*
0.0760.01
WP
CHO-E
6.061.1
3.360.8
0.960.3†
Values are means 6 SE. Na1 and K1 fluxes also represent movement of Cl2 with each respective cation. Units are meq · cm21 · h21 for Na1
and K1, and mmol · cm21 · h21 for CHO. Negative values represent secretion. * Significantly different from WP. † Significantly different from 0to 25-cm segment.
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Fig. 4. Total solute flux in 3 segments of proximal small intestine.
Values are means 6 SE.
ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
mosmol/kgH2O at 25 cm. Corresponding values for the
CHO-E beverage were 252 6 5 and 278 6 3 mosmol/
kgH2O, respectively (Fig. 5). Luminal [Na1] was virtually identical between solutions at the beginning of the
duodenum but rose significantly higher during ingestion of the WP compared with the CHO-E beverage
(Fig. 6). This elevation in [Na1] is due to greater Na1
secretion and/or greater water absorption. Because net
Na1 flux in the duodenum was essentially zero (Table 2)
and net water flux was significantly greater for the WP
than the CHO-E beverage, the higher [Na1] in the first
25 cm is attributable to initial Na1 secretion and a high
rate of water movement down an osmotic gradient of
Fig. 7. Potassium concentration in stomach and various segments of
proximal small intestine. Values are means 6 SE. * Significantly
different from WP, P , 0.05. # Significantly different from stomach
site, P , 0.05. †Significantly different from 0-cm site, P , 0.05.
& Significantly different from 25-cm site, P , 0.05.
Fig. 8. Percent change in plasma volume during 85 min of cycle
ergometry at 60–65% peak O2 uptake while subjects ingested either
WP or a 6% CHO-E beverage. Values are means 6 SE.
,130–230 mosmol/kgH2O. Net water absorption in the
presence of Na1 secretion has also been observed in the
proximal small intestine by Santangelo and Krejs (45).
K1 fluxes were negligible in both trials and did not
contribute substantially to TSF.
Water absorption values obtained in the 0- to 25-cm
segment contrast with those previously observed during
segmental perfusion of the duodenojejunum. Perfusion
of distilled water (infusion rate 5 15 ml/min) in the
distal duodenum and proximal jejunum during both rest
and exercise (70% V̇O2 peak) in two previous investigations (20, 23) produced significantly lower fluid absorption rates (,8–9 ml · cm21 · h21 ) compared with a CHO-E
solution similar to that used in this investigation
(,12–13 ml · cm21 · h21 ). In the present study, water
flux in the duodenum was 30 vs. 15 ml · cm21 · h21 for
WP and CHO-E, respectively. This discrepancy is attributable to the intestinal segment studied. In the previous reports, the test segment under study consisted
primarily of the jejunum. In this, and one other recent
study (44), water absorption was greater when the
duodenum was studied. Reitemeier et al. (42) also observed rapid rates of water absorption (50% in 3 min
and 67% in 5 min) in the distal duodenum/proximal
jejunum after infusion of labeled water (isotopic tracer
method using D2O) into the duodenum. These rates
closely resemble those of the present study (for WP,
,60% total volume absorbed in 0- to 25-cm segment).
In addition, Shi et al. (49) reported water flux for a
hypotonic solution exhibited the highest water absorption rates, followed by isotonic and hypertonic solutions, when water flux in the duodenum and jejunum
was combined. In contrast, Santangelo and Krejs (45)
perfused the stomach with water at 22 ml/min and
examined water absorption in a 50-cm mixing segment,
70-cm jejunal test segment, and 70-cm ileal test segment. Their results indicated higher water absorption
in the jejunum (7.2 ml · cm21 · h21 ) vs. mixing segment
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Fig. 6. Sodium concentration in stomach and various sites in proximal small intestine. Values are means 6 SE. * Significantly different
from CHO-E, P , 0.05. # Significantly different from stomach value,
P , 0.05. †Significantly different from 0-cm site value, P , 0.05.
& Significantly different from 25-cm site, P , 0.05.
209
210
ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
[3.8 ml · cm21 · h21 (presumably duodenum)] and the
ileum (2.0 ml · cm21 · h21 ). However, because their 50-cm
mixing segment ended at the ligament of Treitz (start of
the jejunum), and given that the duodenum is only
,25 cm long (10, 33), the other 25 cm of this segment
must have been in the stomach. Thus mixing segment
water absorption actually occurred in ,25 cm rather
than 50 cm, elevating water absorption in the duodenum to ,7.6 ml · cm21 · h21, which is approximately the
same as that found in the jejunum.
Higher water absorption values in this study compared with those in others may also reflect high GE
rates (,18–19 ml/min), which served as the infusion
rate when water flux was calculated (52). Most investigators who use segmental perfusion employ infusion
rates of 10–15 ml/min.
Jejunal Absorption (25–50 cm and 50–75 cm)
uptake is greater in jejunal compared with
duodenal brush border membrane vesicles.
By the final 25-cm segment (50–75 cm), 66% of the
WP and 53% of the CHO-E beverage were absorbed,
which presumably reduced the flow rate of each to this
segment and explains the significant decline in fluid
absorption compared with their highest values (0- to
25-cm segment). Furthermore, the osmotic gradient
basically disappeared by the end of this segment for the
WP beverage (WP 5 ,260 mosmol/kgH2O; Fig. 5).
There were no differences between the two beverages
for fluid absorption in this segment. In the entire 75-cm
segment, ,75% of the ingested volume of each solution
(minus volume withdrawn for sampling) was absorbed
with no differences in total water absorption between
solutions.
Using the isotopic tracer technique (D2O), Davis et al.
(12) also observed similar rates of fluid replacement
between an isotonic CHO-E beverage and distilled
water during cycle exercise in the heat (2 h at 75%
V̇O2 peak; 27°C) . In contrast, Leiper et al. (30) and Davis
(11) found that isotonic CHO-E solutions were absorbed
more readily than water in resting subjects by using
this method. It is important to note that isotopic tracer
studies do not examine net flux of fluid, only unidirectional flux from intestinal lumen to blood.
It is apparent that had the jejunum been studied
exclusively, and the duodenum bypassed, the present
results would have been misleading. Interpretation of
absorptive efficacy of the beverages (on the basis of only
jejunal data) would have favored the CHO-E beverage.
However, when duodenal data are considered, fluid
absorption was greater for the WP, and thus overall
absorption of each beverage indicates no distinct advantage for either.
Gastric Influence
Individual GE rates served as infusion rates to
calculate water and solute flux. Mean gastric volumes
of ,250 ml maintained GE rates of 18–19 ml/min,
which agree with other studies using this technique
(28, 44) and are comparable with other repeateddrinking studies (34, 40, 41, 43). These rates were
somewhat higher than infusion rates in most segmental perfusion studies (i.e., 10–15 ml/min). As previously
noted, this may increase water and solute absorption in
the intestine (52). Maintenance of a moderate to high
gastric volume ensures a high rate of GE (38). For
instance, Mitchell and Voss (34) reported a GE rate of
18.9 ml/min after ingestion of ,430 ml of a 7.5% CHO
solution every 15 min during 2 h of cycle exercise at
70% V̇O2 peak. Rehrer et al. (40, 41) report emptying rates
of 14–16 ml/min with ingestion of 8 ml/kg initially
(,600 ml) and 2–3 ml/kg (,150–200 ml) at 20-min
intervals of a 4.5% glucose solution, an isotonic sucrose
(6%) drink, or water during cycling at 70% V̇O2 peak.
Subjects in a study by Ryan et al. (43) emptied 5% CHO
solutions at rates .16 ml/min while ingesting 350 ml
every 20 min during cycling for 3 h at 60% V̇O2 peak in the
heat. Although maximal GE rates are not known,
Costill and Saltin (4) induced average GE rates of
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Net fluid absorption significantly decreased for the
WP beverage in the second 25-cm segment of the
intestine but remained unchanged for the CHO-E
beverage, resulting in significantly more fluid absorption from the CHO-E. This finding is attributable to
three factors: 1) the WP had a lower flow rate to this
segment due to higher water absorption in the duodenum; 2) the osmotic gradient for the WP was reduced
compared with the duodenum (,100 mosmol/kgH2O
increase in luminal osmolality from the proximal sampling site in the duodenum to proximal sampling site in
the jejunum; Fig. 5); and 3) the WP did not contain
CHO, which limited total solute absorption compared
with the CHO-E beverage (Fig. 4). Other studies have
also found CHO-E solutions to be absorbed faster than
plain water in the jejunum (20, 23, 31). This finding is
attributable to enhanced passive water movement in
response to increased net solute absorption. Solute flux
values are shown in Table 2 (Na1, K1, and CHO) and
Fig. 4 (TSF). As expected, the CHO-E beverage produced greater TSF, the majority coming from CHO
absorption, allowing sustained fluid absorption in the
jejunum compared with the WP. This has been termed
‘‘solute drag,’’ ‘‘solvent drag,’’ and solution drag and was
first proposed by Curran (8) and Curran and Macintosh
(9). Schedl and Clifton (46), Sladen and Dawson (53),
and Fordtran (16) further demonstrated the stimulatory effect of glucose on Na1 and water transport in the
jejunum. Recently, Fine et al. (15) reported that the
mechanisms responsible for this increased absorption
are 1) forceful osmotically driven water movement that
‘‘pulls’’ small hydrophilic solutes through trans- and/or
paracellular routes (i.e., solvent drag), and 2) the
creation of a concentration gradient (created by osmotically driven water absorption) that allows for passive
solute movement independent of water flow. Shi et al.
(50) have also reported a close relationship between
water absorption and solute absorption in the duodenojejunum, especially when multiple transportable substrates are present (i.e., glucose, sucrose, glycine, Na1 ).
The maintenance of fluid and solute absorption in this
segment for the CHO-E beverage can also be explained
by the findings of Harig et al. (24), who showed that
D-glucose
ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
25 ml/min after a single bolus (600 ml) of a hypotonic
(,200 mosmol/kgH2O) solution. Duchman et al. (14)
observed GE rates for water of .40 ml/min after
infusion of 750 ml into the stomach with subsequent
infusions of ,180 ml every 10 min. Rates of gastric
secretion in the present study were minimal for both
solutions (26.0 6 7.1 vs. 23.7 6 10.8 ml/10 min for WP
and CHO-E, respectively). These rates compare favorably with other recent studies using similar solutions
(28, 35) and likely did not significantly impact GE.
Furthermore, after a 35-min equilibration period, gastric secretions did not significantly alter the osmolality,
[Na1], or [K1] of the ingested solutions (Figs. 6–8).
Fluid Homeostasis, Thermoregulation,
and Substrate Availability
tion. Furthermore, these data argue for the inclusion of
the duodenum in segmental perfusion studies designed
to evaluate the efficacy of oral rehydration solutions
because this segment of the intestine plays such a
crucial role in fluid absorption. Finally, conclusions
drawn from studies that only examine jejunal absorption of a beverage may be misleading when extrapolated to assess the overall effect on fluid homeostasis
with oral ingestion of the same beverage.
The authors thank the subjects for participating in the experiments, Joan Seye for assistance in manuscript preparation, and Pat
Johnston, Shawn Fleck, Kay Pals, and Tonya Brueggeman for
technical assistance.
This study was supported by the Gatorade Sports Science Institute.
Address for reprint requests: C. V. Gisolfi, Dept. of Exercise
Science, N414 Field House, Univ. of Iowa, Iowa City, IA 52242-1111.
Received 25 November 1996; accepted in final form 18 March 1997.
REFERENCES
1. Barclay, G. R., and L. A. Turnberg. Effect of moderate exercise
on salt and water transport in the human jejunum. Gut 29:
816–820, 1988.
2. Beckers, E. J., N. J. Rehrer, F. Brouns, F. T. Hoor, and
W. H. M. Saris. Determination of total gastric volume, gastric
secretion and residual meal using the double sampling technique
of George. Gut 29: 1725–1729, 1988.
3. Cooper, H., R. Levitan, J. S. Fordtran, and R. J. Ingelfinger. A method for studying absorption of water and solute from
the human small intestine. Gastroenterology 50: 1–7, 1966.
4. Costill, D. L., and B. Saltin. Factors limiting gastric emptying
during rest and exercise. J. Appl. Physiol. 37: 679–683, 1974.
5. Coyle, E. F., A. R. Coggan, M. K. Hemmert, and J. L. Ivy.
Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J. Appl. Physiol. 61: 165–172, 1986.
6. Coyle, E. F., J. M. Hagberg, B. F. Hurley, W. H. Martin, A. A.
Ehsani, and J. O. Holloszy. Carbohydrate feeding during
prolonged strenuous exercise can delay fatigue. J. Appl. Physiol.
55: 230–235, 1983.
7. Coyle, E. F., and S. J. Montain. Carbohydrate and fluid
ingestion during exercise: are there trade-offs? Med. Sci. Sports
Exerc. 24: 671–678, 1992.
8. Curran, P. F. Na, Cl and water transport by rat ileum in vitro. J.
Gen. Physiol. 43: 1137–1148, 1960.
9. Curran, P. F., and J. R. Macintosh. A model system for
biological water transport. Nature 193: 347–348, 1962.
10. Davenport, H. W. Motility of the small intestine. In: Physiology
of the Digestive Tract (5th ed.), edited by H. W. Davenport.
Chicago, IL: Year Book, 1983, p. 70–97.
11. Davis, J. M., D. R. Lamb, W. A. Burgess, and W. P. Bartoli.
Accumulation of deuterium oxide in body fluids after ingestion of
D2O-labeled beverages. J. Appl. Physiol. 63: 2060–2066, 1987.
12. Davis, J. M., D. R. Lamb, R. R. Pate, C. A. Slentz, W. A.
Burgess, and W. P. Bartoli. Carbohydrate-electrolyte drinks:
effects on endurance cycling in the heat. Am. J. Clin. Nutr. 48:
1023–1030, 1988.
13. Dill, D. B., and D. L. Costill. Calculation of percentage changes
in volumes of blood, plasma, and red cells in dehydration. J.
Appl. Physiol. 37: 247–248, 1974.
14. Duchman, S. M., T. L. Bleiler, H. P. Schedl, R. W. Summers,
and C. V. Gisolfi. Effects of gastric function on intestinal
composition of oral rehydration solutions. Med. Sci. Sports Exerc.
22: S89, 1990.
15. Fine, K. D., C. A. S. Ana, J. L. Porter, and J. S. Fordtran.
Mechanism by which glucose stimulates the passive absorption
of small solutes by the human jejunum in vivo. Gastroenterology
107: 389–395, 1994.
16. Fordtran, J. S. Simulation of active and passive sodium absorption by sugars in the human jejunum. J. Clin. Invest. 55:
728–737, 1975.
Downloaded from http://jap.physiology.org/ by 10.220.32.247 on June 18, 2017
Whereas water absorption differed among the intestinal segments and solutions in certain segments, there
were no differences in overall water retention, percent
change in plasma volume (Fig. 8), or plasma osmolality.
Nor were differences observed between solutions for
sweat rate, percent body weight loss, urine production,
final rectal temperature, or final heart rate (Table 1).
Within the 75-cm segment studied, our calculations
accounted for the absorption of 83 vs. 72% of the
ingested volume for the WP and CHO-E beverages,
respectively. After urine production was substracted
from results of each trial, 80 and 82% of the absorbed
volume was retained for WP and CHO-E trials, respectively. This indicates that although the WP beverage
was absorbed earlier in the small intestine than the
CHO-E beverage, it does not improve fluid homeostasis
or thermoregulatory function compared with the CHO-E
beverage. Segmental perfusion data do not indicate the
overall efficacy of a beverage. Studies examining intestinal absorption should also determine fluid retention
together with plasma volume changes, and possibly
body fluid shifts.
Plasma glucose concentrations were significantly
lower throughout exercise in the WP compared with the
CHO-E trial. Absorption of CHO by all segments of the
intestine in the CHO-E trial promoted maintenance of
plasma glucose concentrations throughout the experiment. Eighty-eight grams of CHO were absorbed within
the 75-cm segment studied, or ,1 g/min. This rate
meets the maximal blood glucose oxidation rate during
prolonged exercise (25). Although performance was not
measured in these experiments, ingestion of CHOcontaining solutions during prolonged exercise can
improve endurance and enhance performance probably
through the maintenance of plasma glucose concentration (5–7, 12, 36, 37).
In summary, significant differences exist in intestinal
absorption between solutions and among segments in
the proximal small intestine. In the duodenum, fluid
from the WP beverage is absorbed quickly by movement down a large osmotic gradient despite the possibility of electrolyte secretion. In the jejunum, fluid absorption from the WP beverage is significantly reduced
compared with the CHO-E solution, which stimulates
greater solute flux, thus promoting greater fluid absorp-
211
212
ABSORPTION FROM DIFFERENT INTESTINAL SEGMENTS DURING EXERCISE
35. Murray, R., D. E. Eddy, W. P. Bartoli, and G. L. Paul. Gastric
emptying of water and isocaloric carbohydrate solutions consumed at rest. Med. Sci. Sports Exerc. 26: 725–732, 1994.
36. Murray, R., D. E. Eddy, T. W. Murray, J. G. Seifert, G. L.
Paul, and G. A. Halaby. The effect of fluid and carbohydrate
feedings during intermittent cycling exercise. Med. Sci. Sports
Exerc. 19: 597–604, 1987.
37. Murray, R., J. G. Seifert, D. E. Eddy, G. L. Paul, and G. A.
Halaby. Carbohydrate feeding and exercise: effect of beverage
carbohydrate content. Eur. J. Appl. Physiol. 59: 152–158, 1989.
38. Noakes, T. D., N. J. Rehrer, and R. J. Maughan. The
importance of volume in regulating gastric emptying. Med. Sci.
Sports Exerc. 23: 307–313, 1991.
39. Phillips, S. F., and W. H. J. Summerskill. Water and electrolyte transport during maintenance of isotonicity in human
jejunum and ileum. J. Lab. Clin. Med. 70: 686–698, 1967.
40. Rehrer, N. J., F. Brouns, E. J. Beckers, F. TenHoor, and
W. H. M. Saris. Gastric emptying with repeated drinking during
running and bicycling. Int. J. Sports Med. 11: 238–243, 1990.
41. Rehrer, N. J., A. J. M. Wagenmakers, E. J. Beckers, D.
Halliday, J. B. Leiper, F. Brouns, R. J. Maughan, K. Westerterp, and W. H. M. Saris. Gastric emptying, absorption, and
carbohydrate oxidation during prolonged exercise. J. Appl.
Physiol. 72: 468–475, 1992.
42. Reitemeier, R. J., C. F. Code, and A. L. Orvis. Comparison of
rate of absorption of labeled sodium and water from upper small
intestine of healthy human beings. J. Appl. Physiol. 10: 256–260,
1957.
43. Ryan, A. J., T. L. Bleiler, J. E. Carter, and C. V. Gisolfi.
Gastric emptying during prolonged cycling exercise in the heat.
Med. Sci. Sports Exerc. 21: 51–58, 1989.
44. Ryan, A. J., G. P. Lambert, X. Shi, R. T. Chang, R. W.
Summers, and C. V. Gisolfi. Effect of hypohydration on gastric
emptying and intestinal absorption during exercise. FASEB J. 9:
1692, 1995.
45. Santangelo, W. C., and G. J. Krejs. Absorption of pure water
by the human gastrointestinal tract (Abstract). Gastroenterology
88: 1569, 1985.
46. Schedl, H. P., and J. A. Clifton. Solute and water absorption by
the human small intestine. Nature 199: 1264–1267, 1963.
47. Schedl, H. P., R. J. Maughan, and C. V. Gisolfi. Intestinal
absorption during rest and exercise: implications for formulating
an oral rehydration solution (ORS). Med. Sci. Sports Exerc. 26:
267–280, 1994.
48. Schedl, H. P., D. Miller, and D. White. Use of polyethylene
glycol and phenol red as unabsorbed indicators for intestinal
absorption studies in man. Gut 7: 159–163, 1966.
49. Shi, X., R. W. Summers, H. P. Schedl, R. T. Chang, G. P.
Lambert, and C. V. Gisolfi. Effects of solution osmolality on
absorption of select fluid replacement solutions in human duodenojejunum. J. Appl. Physiol. 77: 1178–1184, 1994.
50. Shi, X., R. W. Summers, H. P. Schedl, S. W. Flanagan, R. T.
Chang, and C. V. Gisolfi. Effects of carbohydrate type and
concentration and solution osmolality on water absorption. Med.
Sci. Sports Exerc. 27: 1607–1615, 1995.
51. Sladen, G. E. Absorption of fluid and electrolyte in health and
disease. In: Intestinal Absorption in Man, edited by I. McColl and
G. E. Sladen. London: Academic, 1975, p. 51–98.
52. Sladen, G. E., and A. M. Dawson. Effects of flow rate on the
absorption of glucose in a steady state perfusion system in man.
Clin. Sci. (Lond.) 36: 133–145, 1969.
53. Sladen, G. E., and A. M. Dawson. Interrelationships between
the absorptions of glucose, sodium and water by the normal
human jejunum. Clin. Sci. (Lond.) 36: 119–132, 1969.
54. Whalen, G. E., J. A. Harris, J. E. Geenen, and K. H. Soergel.
Sodium and water absorption from the human small intestine.
Gastroenterology 51: 975–984, 1966.
Downloaded from http://jap.physiology.org/ by 10.220.32.247 on June 18, 2017
17. Fordtran, J. S., and B. Saltin. Gastric emptying and intestinal
absorption during prolonged severe exercise. J. Appl. Physiol. 23:
331–335, 1967.
18. George, J. D. New clinical method for measuring the rate of
gastric emptying: the double sampling test meal. Gut 9: 237–242,
1968.
19. Gisolfi, C. V., and S. M. Duchman. Guidelines for optimal
replacement beverages for different athletic events. Med. Sci.
Sports Exerc. 24: 679–687, 1992.
20. Gisolfi, C. V., K. J. Spranger, R. W. Summers, H. P. Schedl,
and T. L. Bleiler. Effects of cycle exercise on intestinal absorption in humans. J. Appl. Physiol. 71: 2518–2527, 1991.
21. Gisolfi, C. V., R. Summers, and H. Schedl. Intestinal absorption of fluids during rest and exercise. In: Perspectives in Exercise
Science and Sports Medicine. Fluid Homeostasis During Exercise, edited by C. V. Gisolfi and D. R. Lamb. Indianapolis, IN:
Benchmark, 1990, p. 129–180.
22. Gisolfi, C. V., R. W. Summers, H. P. Schedl, and T. L. Bleiler.
Intestinal water absorption from select carbohydrate solutions in
humans. J. Appl. Physiol. 73: 2142–2150, 1992.
23. Gisolfi, C. V., R. W. Summers, H. P. Schedl, T. L. Bleiler, and
R. A. Oppliger. Human intestinal water absorption: Direct vs.
indirect measurements. Am. J. Physiol. 258 (Gastrointest. Liver
Physiol. 21): G216-G222, 1990.
24. Harig, J. M., K. H. Soergel, J. Barry, and K. Ramaswamy.
Brush border membrane vesicles formed from human duodenal
biopsies exhibit Na1-dependent concentrative L-leucine and Dglucose uptake. Biochem. Biophys. Res. Commun. 156: 164–170,
1988.
25. Hawley, J. A., S. C. Dennis, and T. D. Noakes. Carbohydrate,
fluid, and electrolyte requirements during prolonged exercise. In:
Sports Nutrition. Minerals and Electrolytes, edited by C. V. Kies
and J. A. Driskell. Boca Raton, FL: CRC, 1995, chapt. 19, p.
235–265.
26. Hunt, J. B., A. V. Thillainayagam, A. F. M. Salim, S.
Carnaby, E. J. Elliott, and M. J. G. Farthing. Water and
solute absorption from a new hyppotonic oral rehydration solution: evaluation in human and animal perfusion models. Gut 33:
1652–1659, 1992.
27. Hyden, S. A turbidimetric method of determination of higher
polyethylene glycols in biological materials. Ann. R. Agric. Coll.
Sweden 22: 139–145, 1955.
28. Lambert, G. P., R. T. Chang, D. Joensen, X. Shi, R. W.
Summers, H. P. Schedl, and C. V. Gisolfi. Simultaneous
determination of gastric emptying and intestinal absorption
during cycle exercise in humans. Int. J. Sports Med. 17: 48–55,
1996.
29. Leiper, J. B. Absorption of water and electrolytes from hypotonic, isotonic, and hypertonic solutions (Abstract). Proc. Nutr.
Soc. 45: 78A, 1986.
30. Leiper, J. B., A. E. Fallick, and R. J. Maughan. Comparison
of water absorption from an ingested glucose/electrolyte solution
(ges) and potable water using a tracer technique in healthy
volunteers. Clin. Sci. (Lond.) 4, Suppl. 18: 68P, 1988.
31. Leiper, J. B., and R. J. Maughan. Absorption of water and
electrolytes from hypotonic, isotonic and hypertonic solutions. J.
Physiol. (Lond.) 373: 90P, 1986.
32. Malawer, S. J., and D. W. Powell. An improved turbidimetric
analysis of polyethylene glycol utilizing an emulsifier. Gastroenterology 53: 250–256, 1967.
33. McGuigan, J. E., and M. E. Ament. The stomach and duodenum. Anatomy, embryology, and developmental anomalies. In:
Gastrointestinal Disease. Pathophysiology Diagnosis Management (3rd ed.), edited by M. H. Sleisenger and J. S. Fordtran.
Philadelphia, PA: Saunders, 1983, p. 505–521.
34. Mitchell, J. B., and K. W. Voss. The influence of volume on
gastric emptying and fluid balance during prolonged exercise.
Med. Sci. Sports Exerc. 23: 314–319, 1991.