Effect of obesity and major weight reduction on gastric emptying

Abstract

BACKGROUND: An enhanced gastric emptying rate might reduce the satiating effect of food and thereby promote obesity. Gastric emptying rate has previously been compared between obese and lean subjects with conflicting outcome.

OBJECTIVE: Comparison of gastric emptying rate in lean and obese subjects before and after a major weight reduction.

DESIGN: The study was designed as a case–control study comparing obese and lean subjects and a subsequent comparison of obese subjects before and after a dietary induced major weight reduction.

METHOD: Gastric emptying rate following a solid test meal was estimated scintigraphically for 3 h using the left anterior oblique projection.

SUBJECTS: Nineteen non-diabetic obese (mean BMI=38.7 kg/m2) and 12 lean (mean BMI=23.1 kg/m2) males matched for age and height. All obese subjects were re-examined after a mean weight loss of 18.8 kg (95% CI, 14.4–23.2) achieved by 16 weeks of dietary intervention followed by 8 weeks of weight stability.

RESULTS: When comparing obese and lean subjects no differences were seen in overall 3 h emptying rate (30.3% per hour vs 30.5% per hour). However, a trend towards a higher percentage gastric emptying during the initial 30 min was seen in the obese when compared to lean subjects (24.0% vs 17.8% of the test meal; P=0.08). Weight loss was associated with a reduction in percentage gastric emptying during the initial 30 min (from 24.0% to 18.3% of the test-meal; P<0.02), whereas the overall 3 h emptying rate was unaffected (30.3% vs 30.9% per hour). Neither initial or overall emptying rate differed between reduced-obese and lean subjects.

CONCLUSION: Overall 3 h gastric emptying rate was similar in obese and normal weight males, and unaffected by a major weight loss. However, percentage gastric emptying during the initial 30 min for a solid meal appeared to be increased in obese males and was normalized after a major weight reduction.

Introduction

The prevalence of obesity is rapidly increasing worldwide.1 Low physical activity and consumption of highly palatable foods with high energy density seem to play a major role in the development of obesity.2 However, some individuals appear to be more susceptible to the so-called ‘Western lifestyle’ than others, and a number of hereditary dysfunctions are expected to play a role in determining who will become obese.3,4 Gastric distention, in combination with delivery of nutrients to the small intestine, is supposed to contribute to satiety in both animals and humans.5,6 An enhanced gastric emptying might predispose to overeating and obesity.7 In agreement with this theory, lean to slightly overweight Mexican Americans, a population known to be susceptible to obesity, have an enhanced gastric emptying rate compared to non-Hispanic Whites matched for age, gender and body mass index (BMI).8 More recently, results presented by Näslund et al have indicated an increased rate of emptying of the first 50% of a solid meal (T50) in morbidly obese compared with lean subjects matched for age and sex.9 These and similar findings10,11 are, however, challenged by others who found a similar12,13,14,15 or even a slower gastric emptying in obese individuals.16,17,18 Most of these studies have only compared obese and lean subjects, and have involved somewhat inconsistent group-matching and subject standardization.12,14,15,16,17,18 Few studies have examined the effect of a major weight loss on gastric emptying rate, and these studies do not include a period of weight maintenance prior to the re-examination in order to distinguish the effect of a weight loss per se from the effect of the energy restriction that induced the weight loss.9,10,13

The aim of this study was to compare both percentage gastric emptying during initial 30 min and overall 3 h gastric emptying rates for a solid test meal, estimated scintigraphically, in obese and lean men matched for age, height and standardized with respect to weight stability prior to the examination and to re-examine weight stable obese subjects after a major diet-induced weight loss.

It has for a long time been suggested that lean and obese subjects choose different diet compositions and meal patterns.19,20,21 These theories have, however, not been confirmed by more detailed surveys,22 which might partly be due to the tendency for a more selective and a higher degree of under-reporting in obese subjects.19,22,23 However, such differences are still expected to be involved in the development and maintenance of obesity per se and to account for some of the differences in metabolic profiles and gastrointestinal factors between lean and obese subjects. In this study we chose to standardize the diet for one day prior to the examination in order to account for day-to-day variations in diet and meal patterns without abolishing the possible effect of the habitual diet habits on gastric emptying.24,25

Subjects and methods

Subjects

Thirty-five healthy male subjects between the age of 18 and 50 y were recruited by newspapers and television or by personal communication. Twenty-three subjects with grade I–III obesity1 were compared with 12 normal weight controls. Four obese subjects did not complete the study and data are presented only for the 19 completers (Table 1). All subjects were Caucasian, non-diabetic, non-smokers and none were competitive athletes. The two groups were matched for height and age, and the obese subjects were controlled for weight-stability every second week during a run-in period of minimum 6 weeks (Figure 1). The maximum weight-excursion during the run-in period was on average zero, and in 16 of the 19 obese subjects the maximal weight change was below 2%. Control subjects were only weighed at the physical examination.

Table 1 Anthropometric characteristics of the subjectsa
Figure 1
figure1

Weight changes in the 19 obese subjects who completed the present study. Fasting body weight was estimated 6–8 weeks prior to the weight loss intervention, at the beginning of the run-in period, after 8 weeks on 4.2 MJ/day, after the following 8 weeks on 6.3 MJ/day and finally after 8 weeks of weight maintenance. Data are mean and 95% CI. Weight was reduced during both of the two different weight loss treatments (P<0.001 for both periods), whereas no significant weight changes were observed during the run-in period or the weight maintenance phase.

None of the subjects used medication, had proteinuria, haematuria or glucoseuria, tested by sticks. Fasting plasma triglycerides, total cholesterol, high density lipoprotein, alanine aminotransferase, aspartate aminotransferase and glucose were within the normal ranges for lean subjects. As expected, these values tended to be slightly increased in obese subjects for whom mean plasma triglycerides was 1.9 mM (range 0.84–3.7), mean total cholesterol was 5.9 mM (range 4.5–7.3), mean alanine aminotransferase was 35.5 U/l (range 14–68), and mean aspartate aminotransferase was 32.3 U/l (range 20–54). In addition, mean high density lipoprotein was 1.1 mM (range 0.63–1.5) in the obese subjects. None of the obese subjects had a fasting glucose above 5.8 mM.

Diet program

The obese subjects were re-examined following a mean maintained weight reduction of 18.8 kg (range 5.3–32.7) or 14.8% (range 4.0–26.6) of their initial body weight (Table 1; Figure 1). The weight reducing diet program consisted of 8 weeks on a strictly controlled 4.2 MJ/day low calorie formula diet (Gerlinéa®, Wasabrød A/S, Skovlunde, Denmark) with five meals of 30 g nutrition powder suspended in 200 ml skimmed milk providing 77.5 g protein, 102 g carbohydrate and 30 g fat. The initial weight reduction phase was followed by 8 weeks of an energy-restricted diet providing 6.3 MJ/day. This diet was based on an educational system, consisting of four colour-coded isoenergetic interchangeable units (250 kJ/60 kcal). Each colour represented a different nutrient composition: blue counters for food rich in protein, green counters for food rich in complex carbohydrate and fibre, yellow counters for foods rich in simple carbohydrate, and red counters for foods rich in fat. Subjects were requested to adhere to a diet of 25 counters per day, of which a maximum of eight red and a minimum of six blue counters should be consumed daily, providing a minimum daily intake of 60 g protein. Subjects were free to distribute the energy intake over the whole day, but they were encouraged not to eat during the evening and night.

Weight maintenance

The weight reduction was followed by an 8 week weight maintenance diet also assisted by the counter system. Energy requirements were estimated by the equations of Klausen et al26 using gender, height, age, body weight, and body composition estimated by bioelectrical impedance27 (Table 1). Even though the equation for estimation of energy requirement was based on 24 h indirect calorimetry measurement with low physical activity, we subtracted 1.25 MJ (five ‘counters’) from the estimated value to counteract for reduced compliance and compensatory drop in metabolic rate due to the preceding 16 weeks weight loss. Maximum weight-change during the maintenance phase was on average +1%, and for 10 of the 19 subjects the maximal weight-change was below 2% (Figure 1). During the whole 24 weeks intervention period the subjects attended the department as outpatients. Groups of five to seven subjects met weekly during the first 8 weeks and every second week during the rest of the intervention. At these meetings subjects were weighed and received nutritional instruction and behavioural therapy by a dietitian.

Drop outs

One obese subject dropped out of the study after a weight loss of 25 kg during the first 8 weeks, informing that he was not able to adhere to the 6.3 MJ/day diet as he began to re-gain weight. Two obese subjects left the study immediately before the re-examination, and re-examination could not be completed in one subject due to severe migraine. The four drop-outs did not differ from the 19 completers with respect to initial anthropometrical measures or weight loss.

Standardization

On the day prior to the examination all subjects adhered to a standardized isocaloric conventional diet, collected at the department and eaten at home. Estimated energy requirement was based on the equation of Klausen et al.26 The estimated values were multiplied by 1.1 for the obese subjects and by 1.2 for normal weight in order account for free-living physical activity. The energy content of the diet was within 0.5 MJ of estimated requirement and had an energy composition of 15% protein, 50% carbohydrate and 35% fat. Energy intake was distributed with 20% at breakfast, 30% at lunch and 50% at afternoon snack and dinner. All meals had the same macro nutrient composition and were eaten at approximately the same time (within a time-span of 1–1 ½ h interval for each meal). Subjects were instructed only to drink tap-water plus decaffeinated tea and coffee. In addition, subjects were instructed not to participate in sports or other forms of strenuous physical activity during the 2 days prior to the examination.

Gastric emptying

After 12 h fasting including water from midnight the subjects arrived at the Department of Clinical Physiology and Nuclear Medicine around 8:30 am having used the least strenuous means of transportation. Between 9:00 and 9:30 am a standardized solid test meal consisting of omelet and 135 g wheat bread as sandwiches with 200 ml tap water was ingested at a steady speed over 8 min. The omelet was prepared from 102 g pasteurized egg white, 37 g pasteurized egg yolk, 28 g 13% fat cream and 0.15 g black crusted pepper. The 2.5 MJ meal consisted of 20 E% protein, 50 E% carbohydrate and 30 E% fat with an energy density of 9.0 kJ/g (corrected for a mean 14% shrinkage in the omelet during preparation of three different portions, estimated by a mean of three). The test-meal was estimated to cover a range of 17.3–21.4% of the daily energy requirement in the lean, 15.7–21.3% in the obese and 16.1–22.1% in the reduced-obese subjects, resulting in a significant difference in the relative size of the meal between obese and lean subjects and in the obese subjects at the first and second examination (P<0.001).

Approximately 60 MBq of 99mTc-labelled sulphur colloid was mixed with the egg mass immediately before cooking. The omelet was prepared by cooking in a microwave oven (3 min at 600 W). Immediately after ingestion of the test meal imaging was performed with the subject in the upright position using a large-field-of-view gamma camera equipped with a low-energy collimator and interfaced with a dedicated computer (StarCam XR/7, Star 4000i, GE Medical Systems, Milwaukee, IL, USA). In order to correct for variations in gamma ray attenuation we used the left anterior oblique projection of the abdominal region during imaging.28 Images were acquired for 120 s every 30 min during the following 3 h. Marks were made on the floor to ensure that each person was placed in front of the gamma camera in the same angle at every measurement. Outside the imaging periods subjects were seated in a waiting room, but were allowed to stand and walk around as they pleased. After the examination, regions of interest were manually drawn around the stomach in each image and the counts were recorded and corrected for physical decay.

Ethics

Informed, written consent was obtained from all subjects after the experimental protocol had been described to them in writing and orally. The study was approved by the local ethical committee in accordance with the Helsinki-II declaration.

Dosimetrical evaluation

The radiation dose from ingestion of 60 MBq of 99mTc-labelled sulphur colloid was estimated to be 1.44 mSv.

Statistics

Overall 3 h gastric emptying rate was calculated separately for each subject by linear regression on the seven repeated measures of percentage of gastric content (StatView SE+GraphicsTM). Emptying in kJ per min was calculated from the observed disappearance of 99mTc from the stomach, as the emptying of the meal was assumed to closely follow the emptying of 99mTc. Area under the curve (AUC) was calculated for the whole 3 h period and for the initial 1 h period. Anthropometrical measures, initial and mean emptying rates as well as AUCs for gastric emptying were compared by independent samples t-test (lean vs obese) and paired t-test (obese before and after weight loss). The gastric emptying curves were compared by a two-factor repeated measurement ANOVA analysis (standard repeated measurement analysis in General Linar Model, SPSS 8.0 for Windows). Pearson's correlation test was used to test for correlations between variables.

Results

No differences were seen in the 3 h overall emptying rate, which was estimated to be 30.3% per h in the obese subjects vs 30.5% per h in lean subjects, corresponding to a mean delivery of 12.6 kJ per min to the small intestine. Likewise AUC for the 3 h period was identical between the two groups (Table 2). However a non-significant higher initial gastric emptying rate was seen in the obese subjects when compared to lean subjects. During the first 30 min 24.0% of the test meal left the stomach in the obese compared to 17.8% in the lean subjects (P=0.08) and also AUC60 min tended to differ between the two groups (P=0.12; Table 2, Figure 2). No differences in the shape of the gastric emptying curves were found when applying a two factor repeated measurement ANOVA.

Table 2 Gastric emptying of a 2.5 MJ solid test meal in lean subjects and in obese subjects before and after a major weight lossa
Figure 2
figure2

Gastric emptying of the 2.5 MJ solid test meal in 12 lean subjects () and 19 obese subjects before (□) and after (*) a major weight loss.

When re-examined after a mean weight loss of 18.8 kg 3 h emptying-rate was 30.9% per h and percentage gastric emptying during initial 30 min was 18.3% (Table 2). The percentage gastric emptying during initial 30 min observed at the re-examination was significantly different from the value before weight reduction (P<0.02, Figure 3). Similarly, AUC60 min was significantly lower after the weight loss compared to the value before weight loss (P<0.03, Table 2). No differences in the shape of the gastric emptying curves were found when applying a two-factor repeated measurement ANOVA.

Figure 3
figure3

Percentage gastric emptying during initial 30 min following the 2.5 MJ solid test meal in 19 obese subjects before and after a mean weight reduction of 18.4 kg.

There was a tendency for an inverse correlation between total weight loss and at reduction in percentage gastric emptying during initial 30 min (P=0.095; r2=0.16) and AUC60 min (P=0.085; r2=0.16).

Discussion

The major result of the present study was that 3 h gastric emptying rate was similar in obese and normal weight males, and unaffected by a major weight loss. However, initial 30 min emptying tended to be enhanced in the obese subjects and it was normalized by weight reduction.

The finding of a similar overall gastric emptying rate of a solid or mixed meal in obese and lean subjects is in agreement with several previous studies,12,13,14,15,29 but seems to contradict several others.9,10,11,16,17,18 These rather conflicting results from previous studies comparing gastric emptying between obese and lean subjects could be ascribed to differences in the degree of group-matching and standardization of subjects. Therefore one of the main purposes of the present study was to optimize group-matching and comparability of measures of gastric emptying rate. Only non-smoking male subjects were included in order to eliminate the potential influence of smoking31,32,33 and gender.29,34,35,36 To reduce the possible influence of anthropometrical factors other than body fatness,37,38,39 the groups were closely matched for height and age. In addition, weight was controlled every second week for a period of minimum 6 weeks in obese subjects in order to minimize weight fluctuations. Because of its composition the solid test-meal was expected to promote a high degree of mixing of labelled and non-labelled components within the stomach, and in size the meal resembled a normal breakfast. As previously mentioned, subjects were standardized in order to minimize the effect of day to day variation in diet and physical activity. All subjects were instructed to abstain from strenuous physical activity for 2 days prior to the examination, and they consumed a standardized weight maintenance diet on the day prior to the examination. Such a standardization should not abolish the previously described effect of different habitual diet, although it might weaken it.24,25,30

Our present study and previous results from Näslund et al9 suggest an enhancement of the initial emptying phase in obese subjects, although with an overall emptying similar to that of lean subjects. It is possible that obese subjects have a higher absorptive capacity in the upper part of the small intestine38 and that the ‘threshold emptying rate’ for activation of negative feedback mechanisms from the small intestine is increased in these subjects. This theory is in agreement with the findings of a low or even lacking increase in plasma concentrations of the ‘ileal break hormone’ glucagon like peptide 1 (GLP-1) in morbidly obese subjects after ingestion of relatively small test breakfast (1.2–1.4 MJ)9,40 and a general reduction of the precursor glicentin when comparing diurnal profiles from obese subjects with those from lean subjects.41 The previous demonstration of an acceleration of the overall emptying rate in obese subjects10,11 could in fact represent an enhancement of the emptying of the first part of a meal or of small meals. The 0.8 MJ test-meal used by Wright must be considered a very small meal, especially for obese subjects with a mean overweight of 77%.11 In the study by Tosetti a 2.7 MJ test lunch was given after 5 h of fasting.10 The size of this test meal was identical to the one used in our study; however, an overestimation of the emptying rate is suggested by the finding of an apparent mean emptying of 19 and 29 kJ per min from the stomach (lean and obese subjects, respectively), which is high compared to the solid emptying rates found in our study and described by others.9,11,15,18,35,42,43 Overestimation of the emptying rate might be due to the fact that the test-meal consisted of a main course of 99 mTc-labelled hamburger served with potatoes plus a non-labelled desert of crème caramel. This procedure could theoretically lead to an estimation of the emptying rate for the first part of the meal rather than an estimation of the overall emptying rate,10 so what is described as an acceleration of the overall gastric emptying in obese subjects might actually represent an enhanced emptying of the part of the meal that is ingested first.

The reason for the previous observations of a reduced gastric emptying rate in obese subjects is not clear, but could be an artefact produced by a low male to female ratio in the obese-group compared to the control group17,18 or the lack of taking into account additional factors such as weight stability, menstrual cycle or smoking.11,16,17,18

We found the initial 30 min emptying rate to be normalized in obese male subjects following a mean weight loss of 18.8 kg or 14.8% of the initial weight. A similar finding of a prolongation and hereby a ‘normalization’ of the lag-phase and half emptying time (T50) in obese subjects following a major weight reduction has previously been described.9 Since delivery of food to the small intestine can constitute part of the mechanism of development of satiety in response to gastric distention,5,6 prolongation of the lag-phase or slowing of the initial emptying rate might postpone meal-termination and thereby pre-dispose to over-consumption and regain of a weight loss.

In agreement with our finding of a similar overall gastric emptying rate before and after a mean weight reduction of 14.8% of the initial weight, the overall gastric emptying rate has previously been found to be unaffected by weight reductions of both 8% and 26%.9,13 However, a significant reduction in overall gastric emptying rate to a rate similar to that observed for lean subjects, has previously been described following a 10% weight reduction.10 However, these results might represent a reduction of the initial, rather than the overall emptying rate, judging from the experimental procedure as discussed above. Finally it should be noted that, in all of these studies, re-examination took place immediately after termination of the weight-reducing diet-intervention, and it is therefore impossible to distinguish between effects of the reduced weight and the possible effects of negative energy balance per se.44,45

Recently, Teff et al have shown that increased activity in the parasympathetic efferent simulation of the stomach might be the mechanism that leads to an increased gastric emptying in obese subjects.29 Another theory is that a higher initial emptying rate in obese individuals is caused by an adaptation to a high energy intake, or a high fat energy percentage.24 Previous studies on lean subjects have suggested a reduction in the sensitivity to the intestinal hormone CCK following 2 weeks of a high fat–high energy diet and thereby a reduced negative feedback on gastric emptying as well as on food intake.46 Normalization of gastric emptying following dietary restriction and subsequent weight loss could therefore be a secondary effect of normalization of CCK sensitivity.46 However, other studies do not support the theory of reduced satiety response to intestinal infusion of nutrients or to intravenous infusion of CCK in obese subjects.47,48 In the present study we failed to find any relation between the change in initial 30 min emptying rate and the weight loss, which suggests that the observed normalization of initial 30 min emptying rate might be ascribed to the change in diet composition during the intervention rather than the induced weight loss per se. Further studies are needed in order to describe the isolated effects of a stabilized weight reduction and the change in eating habits on gastric emptying.

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Acknowledgements

The authors wish to thank Inge Timmermann, Jannie M Larsen, Kirsten B Rasmussen, Bente Knap, Lars Paaske, Ulla Pedersen, Anette Vedelspang and Charlotte Kostecki for expert technical assistance at Research Department of Human Nutrition. We also whish to thank Ingelise Siegumfeldt and laboratory staff at the Department of Clinical Physiology and Nuclear Medicine, Hvidovre Hospital. Finally we wish to thank Wasa Brød A/S (Skovlunde, Denmark) for kindly donating the full supply of the low calorie formula diet Gerlinéa®. This study was supported by the Danish Medical Research Council.

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Verdich, C., Lysgård Madsen, J., Toubro, S. et al. Effect of obesity and major weight reduction on gastric emptying. Int J Obes 24, 899–905 (2000). https://doi.org/10.1038/sj.ijo.0801250

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Keywords

  • gastric emptying rate
  • human
  • male
  • obesity
  • weight loss
  • dietary intervention

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