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Magnetic Resonance Centre, School of Physics and Astronomy, Nottingham NG7 2RD, UK;
*
Division of Gastroenterology and
**
Department of Surgery, Queen’s Medical Centre, University Hospital, Nottingham NG7 2UH, UK; and
Institute of Food Research, Colney, Norwich NR4 7UA, UK
3To whom correspondence and reprint requests should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • meal viscosity • gastric emptying • satiety • humans • echo-planar imaging
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Haskell et al. 1992
, Zavoral et al. 1983
). Several animal
studies have shown that meal viscosity influences gastric motor
function, although the techniques used have involved invasive surgery,
and it is not clear that the results can be applied directly to humans
under normal conditions (Cherbut et al. 1990
,
Prove and Ehrlein 1982
). Human studies suggest that high
viscosity meals are more satisfying (Bergmann et al. 1992
, Di Lorenzo et al. 1988
), and increasing
viscosity may slow gastric emptying (Krotkiewski 1984
,
Sandhu et al. 1987
, Wilmshurst and Crawley 1980
). Testing this hypothesis in humans is difficult without a
technique with which to measure intragastric volumes and viscosity.
Scintigraphic emptying studies (Chaudhury 1974
) have
limited image resolution and cannot be repeated frequently because of
the associated radiation dose. Furthermore, scintigraphic studies
provide information only about the amount of meal remaining in the
stomach, rather than the total gastric volume including secretions,
which is likely to be the critical determinant of satiety.
Ultrasonographic techniques are limited to views of the antrum because
assessment of the whole gastric volume is difficult due to air/fluid
interfaces, which disrupt the ultrasound beam. Recently,
echo-planar magnetic resonance imaging
(EPI)4
has been used extensively to study gastric emptying (Evans et al. 1993
, Schwizer et al. 1992
and 1994
,
Stehling et al. 1989
), motility (Issa et al. 1994
, Schwizer et al. 1996
) and flow
(Boulby et al. 1999
) in the gastric lumen and to obtain
three-dimensional images of the intragastric distribution of
water-containing meals (Wright et al. 1996
). EPI is
an ultrahigh speed magnetic resonance imaging (MRI) (Mansfield 1977
) technique, which can effectively freeze gastric motility;
thus it can overcome abdominal motion artifacts by acquiring images in
130 ms. Assessing the dynamic changes in intragastric meal viscosity
using nasogastric intubation and aspiration is difficult and may modify
normal gastric behavior. It would therefore be of great value to be
able to use EPI to assess the viscosity of gastric contents in vivo,
serially and noninvasively, and to relate this to gastrointestinal
motor function.
We have recently validated a method of measuring the viscosity of a
galactomannan model meal in vitro using EPI (Marciani et al. 1998
). In locust bean gum (LBG) water solutions, the nuclear
spin-spin relaxation process (characterized by the relaxation rate,
T2-1) is dominated
by the fast exchange between the hydroxyl protons on polysaccharide
coils and bulk water (Hills et al. 1991
). Increasing LBG
concentration increases the polysaccharide entanglement, affecting both
the viscosity and the
T2-1 of the solution
and making it possible to calibrate the viscosity of the solution
against its T2-1.
The nuclear magnetic resonance (NMR) and rheological properties of LBG
solutions have also been shown to be independent of exposure to the
intragastric environment (Marciani et al. 1998
). These
characteristics make LBG solutions ideal for carrying out viscosity
measurements in vivo by MRI, provided that an ultrafast imaging
technique is used to overcome gastrointestinal motion.
The first aim of this study was therefore to evaluate the applicability of this novel technique in vivo, by comparing the values of meal viscosity measured by EPI relaxometry within the gastric lumen with the viscosity of retrieved digesta samples measured using a standard viscometer. The second aim was to evaluate the changes in meal viscosity during gastric emptying and correlate them with both meal dilution and the subjective feelings of satiety in normal volunteers.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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LBG (Ceratonia siliqua, food grade, Lucas Meyer
Colloids, Chester, UK) water solutions (0.25, 0.5, 1 and 1.5 g/100 g)
were prepared by adding appropriate amounts of powder and 34
µg phenol red (BDH, Poole, UK) to 800 mL hot water.
The solutions were blended using a food mixer and kept at 90°C for
1 h before being allowed to cool down slowly overnight to 37°C.
The solutions were found to be homogeneous and stable in terms of
relaxation times and viscosity for at least 17 h after
preparation. Phenol red is a nonabsorbable marker, which allows meal
dilution to be measured by spectrophotometry (Hobsley and Silen 1969
).
Healthy volunteers (n = 8), age 18–30 y, 3 men and 5 women, who were free from serious disease, had no history of gastrointestinal disorders and were within ±25% of ideal body weight for their height, attended on four separate experimental morning sessions (>1 d and <7 d apart) after fasting overnight on each occasion. They were intubated with a nasogastric tube (i.d., 4 mm), which was positioned so that its tip was lying on the greater curvature of the stomach with the subject in the left lateral position. Water (50 mL) was then instilled and the positioning of the nasogastric tube within the gastric lumen was verified by recovering at least 45 mL of gastric aspirate (checked using Litmus paper). After this procedure, each volunteer drank 500 mL of one of the four LBG meals, which had been prepared as described above. The time when meal ingestion started was defined as t = 0 min. Meals were given according to a Latin-square randomization design to avoid order effects. This protocol was approved by the University Medical School Ethics Committee, and volunteers gave informed written consent before experiments.
Echo-planar imaging.
Single-shot EPI (Howseman et al. 1988
) images were
acquired on a whole-body 0.5 T purpose-built EPI scanner
equipped with actively shielded gradients and a 50-cm diameter
bird-cage coil. The in-plane resolution was 4.3 mm x 2.6
mm; a slice thickness of 1 cm was used throughout the experiments. Each
image was acquired in 130 ms using a 128 x 128 matrix with an
effective echo time of 40 ms. Initially, T2
data sets were acquired for each meal in vitro at 37°C by using a
spin-echo EPI sequence with eight echo times varying from 60 to 960
ms repeated once. The repetition time was 10 s with a total
acquisition time of 2.7 min. After ingestion, a transverse rapid
multislice set of EPI images of the subject was acquired from the heart
to the kidneys to determine the position and volume of the gastric
lumen. The spin-echo EPI sequence was then used to acquire in vivo
T2 data. Volume and T2 data sets
were acquired every 12 min until the stomach appeared empty. Volunteers
were asked to hold their breath before each image acquisition to
minimize diaphragmatic displacement. In between scanning, volunteers
were asked to sit upright on the scanning bed, lying down only for the
time necessary to acquire the images. The time taken to drink the most
viscous meal was longer than that required to ingest the least viscous
one; thus the acquisition of the first set of images was standardized
to be 12 min after the beginning of ingestion for all meals.
Rheology measurements.
Viscosity measurements were conducted at 37°C using a CSR10 (Bohlin
Instruments, Cirencester, UK) temperature-controlled rheometer.
Samples (20 mL) of the test meal were obtained before ingestion,
immediately after ingestion and 40 min after ingestion with the use of
the nasogastric tube. These samples underwent stress viscometry
measurements with the use of a concentric cylinder geometry probe.
Stress viscometry profiles were acquired for 30 shear rates spaced
logarithmically and ranging from 0.1 s-1 to 1000
s-1. Zero-shear viscosity (
0) values
(in Pa·s) were then obtained from the viscosity/shear-rate profiles
for each sample (Cronakis and Kasapis 1995
).
Spectrophotometry measurements.
A CE 5501 (Cecil Instruments, Cambridge, UK) UV-visible (vis)
spectrophotometer, operating at 37°C, was used to record the visible
absorption at 560 nm of phenol red (Hobsley and Silen 1969
) for all of the samples that had undergone rheological
measurements. Each sample (0.5 mL) was put in a disposable cuvette and
neutralized by adding 1.5 mL of a 25 g/100 g NH4OH water
solution immediately before measurement. The 25 g/100 g
NH4OH water solution was used to zero the spectrophotometer
before each measurement. For each experiment, the values of the
absorption of light at 560 nm by the samples retrieved via the
nasogastric tube at later times were expressed as a proportion of the
values obtained for the meal before ingestion. Because the absorption
is directly proportional to the concentration of phenol red within the
samples, the normalized values thus gave the fractional dilution of the
digesta samples.
Satiety questionnaires.
The feelings of satiety of the volunteers were also assessed using a
self-report scale technique (Hill et al. 1995
).
Before meal ingestion and every 12 min afterwards, volunteers were
asked to give a number between 1 and 10 to indicate the following:
1) how full they felt (1 = "not full," 10
= "extremely full"); 2) how hungry (1 = "not hungry," 10 = "extremely hungry"); and
3) how much food they would eat (1 = "nothing,"
10 = "an enormous meal") at that given time.
Data analysis.
T2 data sets were processed using Analyze
software (Biomedical Imaging Resource, Mayo Foundation, Rochester, MN)
by tracing a region of interest around the meal within the stomach and
then using in-house written software as described previously
(Gowland et al. 1998
). T2 is
the reciprocal of the time constant describing the decline in signal
intensity of the images as the time delay in the imaging sequence
(echo-time) is increased. The T2 values were
converted to viscosity values using a previously established
calibration curve (Marciani et al. 1998
). The
surrounding organs, fat, gastrointestinal gas and the nasogastric tube
were discriminated easily and excluded from the region of interest.
Measurements of the volume of the gastric contents were made by
manually tracing a region of interest around the meal within the
stomach on each slice and summing across the slices to determine the
total volume. The averaged data sets of volume against time were then
analyzed by calculating the half-emptying time
(T1/2) and the area under the
volume-time curve (AUC) (Elashoff et al. 1982
). On
three occasions, subjects failed to swallow all of the 500 mL within
the required time; consequently, some data are missing.
Normal distributions of the data were not assumed, and results are
therefore expressed as medians (range). Statistical analysis was
performed using the nonparametric Friedman two-way ANOVA by ranks,
followed by the Wilcoxon signed-rank test for paired comparisons,
using the Bonferroni correction to adjust the significance obtained for
multiple comparisons. Page’s test for ordered alternatives was used to
test the significance of any trends observed. It tests the hypothesis
of an ordering in the response and is more specific than testing a
difference in the alternatives as in Friedman’s two-way ANOVA
(Siegel and Castellan 1988
). Spearman’s nonparametric
correlation coefficient was used to assess the significance of
associations observed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Before ingestion, the viscosity of the four LBG meals given to
volunteers ranged over four orders of magnitude (Table 1
). Meal T2-1
increased logarithmically with LBG concentration from 0.46 to 0.98
s-1, and the average
T2-1 values before
ingestion differed significantly among different meals (P
< 0.005). The logarithm of rheometer viscosity
(0) of the meal before ingestion was linearly
related to the transverse relaxation rate
T2-1
(s-1) over the range of interest
(r2 = 0.95).
|
Figure 1
shows a multislice set of images acquired across the stomach. It can be
seen that with the EPI sequence, the meal provided contrast sufficient
to discriminate between the stomach contents and the surrounding
tissues without the need for any additional contrast agent.
Figure 2A
shows an example set of in vivo spin-echo EPI images used to
measure the T2 of the meal within the
stomach. The average viscosity (0) values
calculated using EPI in vivo correlated well with average rheometer
measured viscosity 0 values
(r2 = 0.88). (Fig. 2B
).
Viscosity declined immediately after swallowing for the meals because
they were diluted by saliva and by gastric secretions. Although
dilution of each meal was similar, the fall in viscosity of the more
viscous meal was greater because of the exponential relationship
between viscosity and concentration. Immediately after ingestion, the
mean rheometer measured viscosity of the 1.5 g/100 g meal fell from 11
to 2 Pa·s. In contrast, the less viscous 0.25 g/100 g LBG meal showed
a much smaller absolute fall. At 40 min, all of the meals showed a
marked fall in the rheometry-measured viscosity with respect to the
initial value of the corresponding meal (P < 0.05)
(Table 1)
.
|
|
confirmed a
progressive dilution of the stomach contents (Page’s test for trend,
P < 0.01 for all meals), due mainly to the addition of
saliva during swallowing and then to gastric secretions.
Gastric emptying curves were approximately exponential in form for all
of these meals, and the gastric volumes declined rapidly with little
meal remaining after 90 min. The relationship between gastric emptying
time (T1/2) and AUC for the gastric
emptying curve with initial meal viscosity is shown in Table 2
. There was a significant trend (P < 0.05) for the AUC
to increase with initial meal viscosity.
|
). The sense of fullness experienced by volunteers during the emptying
of the LBG meal was significantly influenced by initial meal viscosity
(Friedman ANOVA, 
2 = 9.4, P < 0.02), with a significant trend toward increasing fullness with
increasing initial viscosity (Page’s test for trend, P
< 0.05). Appetite decreased with increasing meal viscosity
(Table 3
). Hunger fell immediately after drinking, especially for the 1 and 1.5
g/100 g LBG meals, but then increased rapidly again. The AUC for hunger
vs. time was significantly related to viscosity (Friedman ANOVA,
2 = 10.4, P < 0.02) with a
significant trend for increasing initial viscosity to be associated
with decreased hunger (Page’s test for trend, P < 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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LBG is a simple galactomannan polysaccharide derived from the endosperm
of the bean; it possesses physical properties that make it particularly
suitable for this study. LBG water solutions are nonnutrient, colorless
and tasteless; in general, they were well tolerated by volunteers.
Liquid solutions of different viscosity can be prepared easily by
varying the concentration. Both the viscosity and MRI parameters of
such a solution depend on the concentration and entanglement of the
polysaccharide coils (Cronakis and Kasapis 1995
), a fact
that allows us to use MRI to assess changes in intragastric viscosity
noninvasively (Marciani et al. 1998
). Importantly for
this study, the viscosity and T2 of
the meal, unlike other viscous gums such as pectin, are unaffected by
pH or gastric juice (Marciani et al. 1998
). The 0.25
g/100 g LBG meal was similar in viscosity to water, whereas the 1.5
g/100 g meal was just pourable and was about the most viscous meal that
could be swallowed. Even so, three subjects experienced nausea and
bloating and failed to drink more viscous meals within the requested
time; however, this may have resulted in part from the discomfort
caused by intubation and the difficulties in swallowing a viscous meal
in the presence of a nasogastric tube. However, previous studies
suggested that a nasogastric tube does not significantly alter gastric
emptying (Müller-Lissner et al. 1982
).
We found a good correlation between viscosity assessed by EPI and
standard bench viscometry. Some scatter will be introduced into the EPI
data by the peristaltic movements, which might move spins out from the
slice of the refocusing pulse, thus reducing the apparent
T2. This could be overcome by using a
thicker slice for the refocusing pulse. Errors in viscometry
measurements performed on the aspirates could arise from small
particulates, which would disturb the rheometer measurements. The four
points that lie above the line of fit on Figure 2B
correspond to data acquired at t = 40 min for the more
viscous meals. This systematic error between the different measures of
viscosity is probably due to underestimation of mean viscosity by the
rheometer measurements because the aspirates will selectively sample
the least viscous part of the meals. Using
T2 mapping, we have subsequently
observed the heterogeneity in meal dilution (Marciani et al. 1999
). Mapping was not performed in this study because of the
presence of the nasogastric tube.
This method allows us to assess meal dilution, gastric distention and
satiety feelings simultaneously, and to relate them to meal viscosity.
An interesting observation made in these experiments was the process of
progressive dilution, which rapidly reduced the viscosity of the LBG
meals. This may be due to either salivation or acid secretion in
response to the meals. Basal acid output of 40–80 mL/h would not be
enough to account for the 150 mL of extra fluid required to produce the
meal dilution we observed, but meal-stimulated secretion, which can
reach 200 mL/h, could easily do so. Salivary output is usually no >75
mL/h, but may increase under the stimulus of a nasogastric tube
(Sonnenberg et al. 1982
). Rapid dilution reduced the
initial large differences in meal viscosity, minimizing the differences
in the gastric emptying rates of these nonnutrient meals. Similar
marked reductions in meal viscosity after ingestion have been observed
previously in rats and in pigs and have been reported to be largely the
result of dilution (Cameron-Smith et al. 1994
,
Cherbut et al. 1990
).
The delayed emptying of the most viscous meals was predictable because
increased viscosity would be expected to reduce flow out of the stomach
given a constant force. However, the stomach probably adjusts to
increased viscosity for the following reason: although viscosity varied
1000-fold between meals, emptying rates differed by a factor of only
1.3. This suggests that the stomach is doing more work in response to
higher viscosity meals; however, models based on flow velocity data are
required to prove this. Whether similar results occur with nutrient
meals remains to be seen because increased outflow resistance due to
pylorospasm and altered duodenal motility is likely to be much more
important than with nonnutrient meals, although models based on
velocity data are required to prove this. Hence, to investigate the
relationship between gastric function and viscous/nutrient meals, we
have recently introduced a nutrient LBG test meal, which has
T2 properties similar to those of the
nonnutrient meal used in this study (Marciani et al. 1999
).
The increased satiety and decreased hunger induced by the more viscous
meals may have been related to the increased gastric volumes and slower
emptying, or to an effect of viscosity on the process of ingestion,
which may alter satiety. or stretch receptors in the stomach. High
fiber meals have been reported previously to be associated with greater
gastric secretion (Grimes and Goddard 1977
), and
increased secretions are known also to be a response to high fiber
diets (Johansen and Bach Knudsen 1994
). This may reflect
in part the cephalic effects of the increased chewing that such meals
require, or it may be a direct response of the oral cavity and gut to
the tactile qualities of the meals (McIntyre et al. 1997
). It is also possible that the stomach alters its
secretions in response to the changes in antral work required to empty
the more viscous meals.
We believe that this novel technique will allow investigation of the relationship between meal viscosity and other aspects of gastrointestinal motor function, such as intragastric flow and motility, which can be monitored noninvasively by MRI. As described here, this technique is limited to model nonnutrient meals, although it can be extended to nutrient and particulate model meals. The use of model meals, rather that real meals, is necessarily artificial, but allows us to separate out the important variables influencing gastric behavior. The technique is well tolerated and could be applied easily to patients with disordered gastric function, including various forms of gastroparesis and non-ulcer dyspepsia. A better understanding of the effects of meal viscosity on satiety and gastric emptying will also be of great importance to the food industry in identifying nonnutrient gums, which could be added to convenience foods to increase the satiety they induce.
|
FOOTNOTES |
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2 Supported by the Biotechnology and Biological
Sciences Research Council (Swindon, UK).
4 Abbreviations used: AUC, area under the curve;
EPI, echo-planar imaging; LBG, locust bean gum; MRI, magnetic
resonance imaging; NMR, nuclear magnetic resonance;
T1/2, half emptying time;
T2, relaxation time;
T2-1, transverse relaxation
rate.
Manuscript received April 28, 1999. Initial review completed June 11, 1999. Revision accepted September 27, 1999.
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C. L. Hoad, P. Rayment, R. C. Spiller, L. Marciani, B. d. C. Alonso, C. Traynor, D. J. Mela, H. P. F. Peters, and P. A. Gowland In Vivo Imaging of Intragastric Gelation and Its Effect on Satiety in Humans J. Nutr., September 1, 2004; 134(9): 2293 - 2300. [Abstract] [Full Text] [PDF]
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D. Geleva, W. Thomas, M. C. Gannon, and J. M. Keenan A Solubilized Cellulose Fiber Decreases Peak Postprandial Cholecystokinin Concentrations after a Liquid Mixed Meal in Hypercholesterolemic Men and Women J. Nutr., July 1, 2003; 133(7): 2194 - 2203. [Abstract] [Full Text] [PDF]
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M. Nishimukai, H. Hara, and Y. Aoyama The Addition of Soybean Phosphatidylcholine to Triglyceride Increases Suppressive Effects on Food Intake and Gastric Emptying in Rats J. Nutr., May 1, 2003; 133(5): 1255 - 1258. [Abstract] [Full Text] [PDF]
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F. Mariotti, M. E Pueyo, D. Tome, R. Benamouzig, and S. Mahe Guar gum does not impair the absorption and utilization of dietary nitrogen but affects early endogenous urea kinetics in humans Am. J. Clinical Nutrition, October 1, 2001; 74(4): 487 - 493. [Abstract] [Full Text] [PDF]
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L. Marciani, P. A. Gowland, A. Fillery-Travis, P. Manoj, J. Wright, A. Smith, P. Young, R. Moore, and R. C. Spiller Assessment of antral grinding of a model solid meal with echo-planar imaging Am J Physiol Gastrointest Liver Physiol, May 1, 2001; 280(5): G844 - G849. [Abstract] [Full Text] [PDF]
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I. Bourdon, B. Olson, R. Backus, B. D. Richter, P. A. Davis, and B. O. Schneeman Beans, as a Source of Dietary Fiber, Increase Cholecystokinin and Apolipoprotein B48 Response to Test Meals in Men J. Nutr., May 1, 2001; 131(5): 1485 - 1490. [Abstract] [Full Text]
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