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Keywords:

  • accommodation;
  • satiety;
  • gastric volume

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Objective: The relationships of gastric accommodation and satiety in moderately obese individuals are unclear. We hypothesized that obese people had increased gastric accommodation and reduced postprandial satiety. The objective of this study was to compare gastric accommodation and satiety between obese and non-obese asymptomatic subjects.

Research Methods and Procedures: In 13 obese (body mass index [BMI] ≥ 30 kg/m2; mean BMI, 37.0 ± 4.9 kg/m2) and 19 non-obese control subjects (BMI < 30 kg/m2; mean BMI, 26.2 ± 2.9 kg/m2), we used single photon emission computed tomography to measure fasting and postprandial gastric volumes and expressed the accommodation response as the ratio of postprandial/fasting volumes. The satiety test measured maximum tolerable volume of ingestion of liquid nutrient meal (Ensure) and symptoms 30 minutes after cessation of ingestion.

Results: Total fasting and postprandial gastric volumes and the ratio of postprandial/fasting gastric volume were not different between asymptomatic obese and control subjects. However, the fasting volume of the distal stomach was greater in obese than in control subjects. Maximum tolerable volume of ingested Ensure and aggregate symptom score 30 minutes later were also not different between obese and control subjects.

Discussion: Asymptomatic obese individuals (within the BMI range of 32.6 to 48 kg/m2) did not show either increased postprandial gastric accommodation or reduced satiety. These datasuggest that gastric accommodation is unlikely to provide an important contribution to development of moderate obesity.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Obesity, defined by an excess of body fat, is a highly prevalent disorder in the Western world. In the United States, it has been estimated that one of three adults is obese (1). Obesity predisposes to, or aggravates, many clinical conditions, such as hypertension, hyperlipidemia, diabetes, gout, atherosclerotic heart disease, restrictive lung disease, gallbladder disease, degenerative arthritis, and infertility (2). Obesity is a multifactorial condition. It is known that genetic, environmental, behavioral, and socioeconomic factors influence food ingestion and determine body weight and adipose tissue mass and distribution (3).

Although the contribution of changes in gastrointestinal motility to the pathogenesis of obesity is unclear, several noteworthy changes in gastrointestinal motility have been observed in obesity (4). For example, some studies suggest more rapid gastric emptying in obesity (5) (6), although normal (7) (8) (9) (10) or even slower (11) (12) (13) emptying has also been reported in other studies. Manometric evaluation of the intraduodenal motility in obese patients has shown disturbances in the interdigestive state with a less frequent occurrence of phase III activity of the migrating motor complex with decreased plasma motilin concentrations (14). Postprandial intestinal transit time in obesity is similar to that in normal weight subjects (9) (15); however, intestinal absorption of nutrients is more efficient in obesity (4) (15).

Using an intragastric balloon, gastric capacity has been shown to be significantly larger in obese than in lean subjects (16) (17) (18), and gastric capacity decreased after a restrictive diet in obese subjects (18). However, most of those studies required insertion of a gastric balloon or tube into the stomach and the maximum water-filled balloon volume was used as an indirect index of gastric capacity. It is unclear whether intubation and placement of the balloon into the stomach may have evoked reflex relaxation of the stomach in these studies (19), or whether obese individuals have a more pronounced reflex relaxation in response to intubation or inflation with an artificial stimulus, that is a balloon, in contrast to the ingestion of a meal. A noninvasive method is required to avoid this reflex response. We developed an approach using99mTc-pertechnetate single photon emission computed tomography (SPECT) imaging of the gastric mucosa followed by image processing and analysis using AnalyzeAVW software (20). This method is noninvasive (20), and it has been validated in healthy subjects in comparison to an intragastric barostat balloon (20) (21). It has been applied to measure stomach volumes and gastric accommodation response defined by the ratio of postprandial/fasting gastric volume in patients who have dyspepsia (22).

We considered the hypothesis that the gastric accommodation response is enhanced in obesity to accommodate large meals and reduce the sensation of postprandial fullness. The feeling of satiety is reported to be less prominent in obese than in normal weight individuals (16). However, the relationships between maximum tolerable volume of food and gastric accommodation are unclear.

Therefore, our aim was to compare the gastric accommodation and satiety responses between moderately obese (body mass index [BMI] ≥ 30 kg/m2) and non-obese (BMI < 30 kg/m2) asymptomatic subjects.

Research Methods and Procedures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Subjects

Thirteen healthy, obese (5 men and 8 women; mean age, 32 ± 8 years; range, 22 to 50 years) and 19 non-obese control (4 men and 15 women; mean age, 35 ± 10 years: range, 19 to 51 years) subjects were recruited from the local community by public advertisement. Obesity was defined as a BMI of 30 kg/m2 or more as suggested by the International Obesity Task Force (23). BMI was calculated as weight in kilograms divided by height in square meters (24). The subjects were screened by means of an abridged bowel disease questionnaire to ensure that they had no gastrointestinal symptoms. The following exclusion criteria were applied: 1) previous abdominal surgery except appendectomy, inguinal hernia repair, or tubal ligation; 2) intake of medications within 48 hours that could alter gastrointestinal motility or satiety (e.g., metoclopramide, proton pump inhibitors, H2 receptor antagonists, anticholinergics, and tricyclic antidepressants, selective serotonin reuptake inhibitors, α-adrenergic agents, and calcium channel blockers); 3) pregnant or lactating; 4) poorly controlled diabetes mellitus; 5) radiation worker; and 6) weight >180 kg (400 lb; because of safety issues related to the weight limits of the SPECT camera used). Women of childbearing potential had a negative pregnancy test within 48 hours before the study.

Study Design

This study was approved by Mayo's Institutional Review Board. All subjects gave signed informed consent and received compensation for participation. The gastric accommodation and satiety tests were performed on two separate days, in the morning after an overnight fast. The moderately obese subjects had an electrocardiogram before the satiety test to screen for possible cardiovascular complications and to verify normal cardiovagal function (beat to beat variability).

Measurement of Gastric Accommodation

We followed methods as previously published (20) (22).

Imaging of Gastric Mucosa.

The gastric mucosa is able to take up and excrete technetium99m (99mTc)-pertechnetate from the circulating blood pool (25). There is evidence that both parietal (oxyntic) cells and nonparietal (mucous) cells are capable of99mTc uptake. This property is now widely used to identify ectopic gastric mucosa in patients with suspected Meckel's diverticulum and retained antral mucosa using radionuclide imaging (25) (26) (27) (28). Uptake of99mTc-pertechnetate is found in all parts of the stomach, although there could be regional differences in radionuclide incorporation due to variations in thickness or surface area of the gastric mucosa (26) (28) (29). In a previous study, Prather et al. (30) administered 5.0 mCi99mTc-pertechnetate intravenously and noted sufficient uptake to allow the entire stomach to be visualized. To ensure sufficient visualization and quantification of volumes on tomographic images, 20 mCi99mTc-pertechnetate was administered intravenously in the study by Kuiken et al. (20). Radiation exposure was within permissible ranges for research and clinical studies.

SPECT Imaging.

Tomographic studies were acquired on a large field of view dual-head γ-camera system (Helix SPECT System; Elscint Ltd., Haifa, Israel) equipped with low-energy, high-resolution collimators. Subjects were positioned supine on the imaging table with the detectors over the upper and mid abdomen to ensure imaging of the stomach and small bowel. Ten minutes after the intravenous injection of 20 mCi99mTc sodium pertechnetate, dynamic tomographic acquisition was performed using the multi-orbit mode of the system. Briefly, in this mode, the system performed three complete 360° orbits at 10 minutes per orbit. For each orbit, images were acquired into a 128 × 128 matrix, every 6° at 3 seconds per image. After completion of the acquisition, orbits could be summed to improve counting statistics. These orbits then were reconstructed using filtered back-projection (Ramp-Butterworth filter, order 10, cutoff 0.45 Nyquist) to produce transaxial images of the stomach. Imaging was performed while subjects were fasting and for 20 minutes after ingestion of a 300-mL Ensure drink (Ross Products, Division of Abbott Laboratories, Columbus, OH) through a straw. One can of Ensure consisted of 8 oz (237 mL), with 250 calories derived from 8.8 g of protein, 6.1 g of fat, and 40 g of carbohydrate. Subjects chose their preferred artificial flavor, chocolate or vanilla.

Gastric volume analysis.

For estimation of gastric volume, the transaxial images were transferred through Digital Image Communications in Medicine to a desktop Windows NT workstation. The stomach was identified in transaxial SPECT images using a semi-automated intensity-based extraction algorithm (Object Extractor, AnalyzeAVW PC 2.5; Biomedical Imaging Resource, Mayo Foundation, Rochester, MN). This software system has been used previously in volumetric imaging studies (25) (27) (31). The semi-automated segmentation algorithm requires the user to identify an appropriate seed point and gray-scale threshold. Three-dimensional renderings of the stomach were produced, and gastric volumes were measured using AnalyzeAVW. Total gastric volume was measured while subjects were fasting and during the two (early and late), 10-minute postprandial periods. To assess volume changes in the proximal and distal regions of the stomach, we arbitrarily divided the stomach by drawing a horizontal line at the lower third point of the longitudinal axis of the stomach and estimated proximal two-third and distal one-third volume of stomach. Volume changes between the fasting and the average of the two postprandial images (expressed as the ratio of postprandial to fasting volumes) were analyzed for statistical differences in obese and control subjects. We have recently demonstrated a highly significant correlation (r = 0.74, p < 0.01) between the accommodation ratios measured by SPECT and by simultaneous intragastric balloon measurement using a barostat (21).

Satiety Test

An adaptation of the method of Tack et al. (32) was used. Briefly, subjects were asked to ingest a nutrient drink (Ensure) at a constant rate of 30 mL per minute. This was regulated by refilling the cup with Ensure using a constant rate perfusion pump (Gemini PC-2; IMED, San Diego, CA). (Subjects were unaware of the volume ingested.) The subjects were instructed to maintain intake at the filling rate. Participants scored their satiety using a graphic rating scale that combines verbal descriptors on a scale of 0 to 5 (0 = no symptoms; 1 = first sensation of fullness [threshold]; 2 = mild; 3 = moderate; 4 = severe; and 5 = maximum or unbearable fullness). Participants were told to stop meal intake when they obtained a score of 5. The maximum volume intake of the nutrient drink was recorded.

Thirty minutes after completing the test, participants were requested to score their symptoms (nausea, bloating, fullness, and pain) using a visual analog scale with 100-mm lines anchored with the words unnoticeable and unbearable at the left and right ends of the lines. The aggregate score was defined as the sum of visual analog scale for each symptom (i.e., maximum of 400). The timing of this symptom assessment was intended to be consistent with previous studies by Tossetti et al. (33) in the literature.

Data and Statistical Analysis

Descriptive statistics were calculated for postprandial stomach volumes and the ratio of postprandial/fasting volumes. Gastric volumes, ratios, and maximum ingested volume were compared between obese and control subjects, using Student's t test. Linear correlations were sought between fasting and postprandial volumes, and maximum tolerable volumes of Ensure or BMI. The α-level for statistical significance was set at 0.05. All statistical analysis was performed by using computer statistical software (SAS Institute Inc., Cary, NC). Before study, the sample size of 13 obese subjects provides >80% power to detect a difference in accommodation response of 25%, which was considered clinically relevant.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Participant Characteristics

Except for weight and BMI, baseline characteristics of obese and control subjects were similar and are shown in Table 1. The mean BMI of the obese subjects was 37 (32.6 to 48) kg/m2 and that of control subjects was 26.2 (20.4 to 29.3) kg/m2. Three (1 man and 2 women) of the 13 obese subjects had BMIs >40 kg/m2.

Table 1.  Baseline characteristics
 Obesity (n = 13)Control (n = 19)p Value
  1. Mean ± SD.

  2. NS indicates not significant.

Men/women5/84/15NS
Age32 ± 835 ± 10NS
Men34 ± 736 ± 10NS
Women31 ± 934 ± 10NS
Height (cm)172 ± 7171 ± 8NS
Men174 ± 7179 ± 6NS
Women171 ± 7169 ± 7NS
Weight (kg)111 ± 2077 ± 11<0.0001
Men112 ± 1787 ± 13<0.05
Women110 ± 2274 ± 9<0.0001
BMI (kg/m2)37.0 ± 4.926.2 ± 2.9<0.0001
Men36.3 ± 3.727.2 ± 2.2<0.005
Women37.4 ± 5.725.9 ± 3.1<0.0001

Gastric Volumes

Fasting and postprandial gastric volumes are shown in Table 2. There were no statistically significant differences of fasting and postprandial gastric volumes (whole stomach or proximal two-thirds of stomach) between the obese and control groups except that the distal gastric volume during fasting was larger in the obese than in the control group (p < 0.05; Figure 1). When corrected for BMI, there was no difference in the distal fasting gastric volume between the two groups.

Table 2.  Fasting and postprandial gastric volumes in obese and control subjects
Gastric volume (cm3)Obesity (men = 5, women = 8)Control (men = 4, women = 15)p Value
  • Mean ± SD.

  • NS indicates not significant.

  • *

    Proximal refers to proximal two-thirds of stomach dividedalong its long axis.

Fasting   
Total217 ± 40208 ± 38NS
Proximal*98 ± 20115 ± 40NS
Distal119 ± 3393 ± 34<0.05
Postprandial   
Total683 ± 87696 ± 102NS
Proximal*394 ± 118415 ± 119NS
Distal289 ± 90281 ± 67NS
image

Figure 1. An example of SPECT image of the stomach in an obese subject. Note a J-shaped stomach and relatively increased size of a horizontally oriented stomach showing a larger distal stomach. Left, fasting image; right, postprandial image. Images are from the same individual.

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The volume change after the 300-mL meal was, on average, ∼200 mL greater than fasting volume plus meal volume, suggesting that the method really measured the accommodation of the stomach to the meal. The median ratio of postprandial/fasting gastric volume in obesity group was 3.39 (range: 2.35 to 4), which was not different from the control group of 3.14 (range: 2.49 to 6.07; Figure 2).

image

Figure 2. The ratio of post-/preprandial gastric volume in obese and control subjects. There was no significant difference between the two groups. Horizontal lines indicate median values. NS = not significant.

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Postprandial Satiety

The maximum ingested volume of the liquid nutrient meal was not different between obese and control subjects (Figure 3). The maximum ingested volumes of the 3 obese subjects with BMIs >40 kg/m2 were 1880, 1726, and 1159 mL, which were all within the limit of mean ± 2 SD (1913 mL) of the control group. Visual analogue aggregate score at 30 minutes was also not different between the two groups (mean score of obesity group: 188; mean score of control group: 194, not significant).

image

Figure 3. Maximum ingested volume of liquid meal in obesity and control subjects. There was no significant difference between the two groups. Horizontal lines indicate median values. NS = not significant.

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Effect of Gender

There were no differences in gastric volumes, ratio of postprandial/fasting gastric volume, and maximum ingested volume between obese men and control men, or between obese women and control women (Table 3).

Table 3.  Gastric volume and maximum ingested volume according to gender in obese and control subjects
 Obesity (men = 5, women = 8)Control (men = 4, women = 15)p Value
  1. NS indicates not significant.

  2. Mean ± SD. Note total volumes of stomach during fasting and postprandially are shown in Table 1; accommodation ratio and maximum volumes ingested for whole group appear in Figures 2 and 3.

Gastric volume (cm3)   
Fasting   
Men229 ± 36217 ± 42NS
Women209 ± 42205 ± 38NS
Postprandial   
Men731 ± 49710 ± 120NS
Women654 ± 95692 ± 102NS
Ratio of postprandial/fasting gastric volume   
Men3.24 ± 0.473.32 ± 0.54NS
Women3.19 ± 0.613.49 ± 0.93NS
Maximum ingested volume (cm3)   
Men1293 ± 2641574 ± 167NS
Women1298 ± 3271266 ± 285NS
Aggregate symptom score at 30 minutes after satiety test (maximum score of 400)   
Men179 ± 77155 ± 24NS
Women195 ± 112205 ± 87NS

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Our results do not support previous studies (16) (17) (18) that reported that the gastric volume is larger in patients with obesity. This discrepancy cannot be completely explained, but the following should be considered. First, most of studies that reported that gastric capacity was larger in obese patients were based on balloon studies, whereas our study involved a noninvasive technique and feeding of a nutrient meal. Gastric capacity in the previous intubated studies may have evaluated the elasticity of the stomach wall because they utilized a distending balloon; these measurements should be distinguished from the gastric volume after a meal. Second, a potential limitation of our study was that the control subjects were somewhat overweight (mean BMI: 26.2 kg/m2), whereas the obese group was moderately, but not morbidly obese (mean BMI: 37.0 kg/m2). The safety limit of load of SPECT camera and the attenuation of the radioisotope by increased body mass influenced our selection of obese subjects. Therefore, additional studies comparing morbidly obese patients (BMI ≥ 40 kg/m2) and lean subjects (BMI < 25 kg/m2) might provide helpful additional information. An intriguing observation in the current study is the presence of a greater distal stomach volume during fasting that seems to be associated with the obesity itself because it is normalized by correcting for BMI.

Our study shows that the SPECT imaging method is able to document the postprandial volume change in excess of the fasting volume plus the 300-mL volume of the liquid nutrient drink. It is also clear that although the liquid drink is being emptied (e.g., in a separate study, a mean of 28% of the same meal had emptied from the stomach during the first 30 minutes postprandially), the volume during the second postprandial 10 minutes was virtually identical (data not shown) to that during the first 10 minutes. This observation, as well as the estimation of volume based on imaging of the gastric wall rather than the gastric content, suggests that SPECT measures gastric capacity, not only the volume ingested. The results show that a gastric accommodation abnormality does not seem likely in obese people; postprandial fullness in asymptomatic people with obesity is not altered relative to controls. Thus, we did not find evidence that obese individuals experienced less postprandial symptoms or tolerated larger meal volume due to greater stomach volume. Our results are in accordance with an invasive measurement of gastric volume and accommodation using a barostat (34). Thus, basal gastric tone and gastric accommodation in response to intragastric balloon distention were not altered in obesity compared with controls. Under physiological conditions, meal ingestion results in a reduction in gastric tone, facilitating the ingestion of large volumes of solids or liquids without inducing symptoms or vomiting (26). This reflex called receptive relaxation or gastric accommodation is a consistent response in health, is prominent in the proximal stomach, and requires intact vagal pathways (35). A reduced accommodation response accounts for postprandial symptoms, such as early satiety and fullness in conditions such as functional dyspepsia (32) (36).

Gastric distention with eating contributes to the feeling of fullness or satiation. The mechanism is unclear, but distending the stomach stimulates gastric stretch receptors, which trigger vagal discharges that activate hypothalamic neurons (37) and induce the feeling of satiety (38). Peptides like leptin, cholecystokinin, and glucagon-like peptide 1 have been shown to evoke satiety, thereby reducing food intake (39) (40).

Some studies (5) (6) have reported accelerated gastric emptying in obesity; this may conceivably result from rapid intragastric meal distribution to the antrum (41) and, hence, not necessitate a large proximal portion of stomach to accommodate the meal. Our study showed larger fasting distal gastric volume in the obese than in the control group. We were intrigued that the mean distal gastric volume was actually larger than the mean proximal volume in the obese group, as measured using an automated algorithm that divided the stomach at the two-third point of its long axis. This difference is not related to body position, because all studies were performed in the supine position. This difference in the size or ratio of the distal to proximal stomach was due to a slender fundus or J-shaped stomach or a horizontally positioned stomach in the obese group. This should be further investigated in a large sample size of participants. We are unable to exclude the possibility that the observed difference may simply reflect orientation of the axis of the stomach in obese people or a simple relationship between organ size and body weight. Additional studies of the relationship among fasting gastric volumes, intragastric meal distribution, gastric accommodation, and postprandial symptoms are needed in a wide range of BMIs.

In our study, the maximum tolerable volume and postprandial symptoms were not different between obese and control subjects. It is important to stress that the maximum tolerable volume of Ensure ingested is not intended as a measure of gastric capacity, because it does not control for the volume of saliva, gastric secretions, or gastric emptying. It was used merely to test the postprandial symptoms after a maximum tolerable load. Even the three morbidly obese subjects (BMI > 40 kg/m2) did not ingest significantly larger volumes of the liquid meal. Furthermore, there was no correlation between gastric volumes and maximum ingested volumes or BMI. Our negative results are similar to those of Geliebter (17) who reported that obese subjects did not ingest more liquid meal than lean subjects when the balloon volume was zero and there was no significant correlation between gastric capacity and intake. Therefore, the satiety mechanism seems to be normal in moderate obesity and eating behaviors, such as more frequent ingestion, periodic binge eating (18), or consumption of a more calorie-dense diet (42) may play a more important role in obesity.

To assess the possibility of a type 2 error in our study, we retrospectively performed power analysis by using our data of control and obese subjects (43). Fourteen subjects in each group were required to demonstrate a 25% difference of the ratio of postprandial/fasting gastric volume or maximum ingested volume of Ensure with a power of 80% and a significance level of 5%. Therefore, our sample size (n = 13 and n = 19) was not likely to result in a type 2 error.

In conclusion, obese patients in our study did not show any gastric accommodation abnormality or reduced postprandial fullness. However, these observations pertain to people in the 32.6- to 48-kg/m2 range of BMI; therefore, additional studies are needed to compare morbidly obese and lean subjects before negating the important observations performed with an intragastric balloon to measure gastric capacity or dismissing a potential role of the reservoir function of the stomach in obesity.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

This study was supported in part by Grants R01 DK-54681-03 (to M.C.), K24 DK-02638-03 (to M.C.), R01 DK-57892-01 (to J.A.M.), and General Clinical Research Center Grant RR00585 from the National Institutes of Health. We thank Cindy Stanislav for typing and preparing this manuscript.

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  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
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