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Keywords:

  • child: dyspepsia;
  • gastric motor function;
  • obesity

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

Background  The aim was to compare gastric emptying rate and nutrient tolerance during a satiety drinking test in children with functional dyspepsia (FD) and obesity and to study the relationship between daily caloric intake and the satiety drinking test.

Methods  A total of 28 dyspeptic children (22 girls, mean age 12.5 ± 3.1 years) and 15 obese children (five girls, 13.3 ± 1.8 years) were studied. The patients underwent an octanoic acid gastric emptying breath test and a satiety drinking test. Prior to both tests, a dyspepsia questionnaire was filled out to calculate the mean calorie intake.

Key Results  The most prevalent dyspeptic symptoms were early satiety (96.4%), postprandial fullness (89.2%), and epigastric pain (78.6%), followed by nausea (50%). All dyspeptic and obese children (= 43) started the satiety drinking test and 41 children completed the test until a score of 5 was reached. The maximum ingested volume in FD was significantly lower than in obesity or in age-matched healthy controls (252 ± 85 vs 479 ± 199 and 359 ± 29 mL respectively, both < 0.05). As a group, dyspeptic children had significantly slower gastric emptying than obese children (89.7 ± 54.8 min vs 72.5 ± 26.0 min, = 0.05). Daily calorie intake was significantly higher in obese children than that in dyspeptic children (2325 ± 469 vs 1503 ± 272 cal, < 0.0001). The endpoint of the satiety drinking test was significantly correlated with body weight or BMI (both R = 0.41, = 0.04), but not with daily calorie intake, gastric emptying rate or age.

Conclusions & Inferences  The satiety drinking test is a potentially useful non-invasive tool in the investigation of children with FD and obesity.


Abbreviations:
BMI

body mass index

FD

functional dyspepsia

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

Food intake is associated with important changes in gastric motor control, aimed at initial storage of the meal, through the gastric accommodation reflex, and subsequent grinding, followed by emptying at a rate that matches small intestinal absorptive capacity.1 In adults, impaired gastric accommodation and delayed gastric emptying have been implicated in the pathogenesis of functional dyspepsia symptoms.2 Abnormalities of gastric motility have also been reported in obese adults, although the contribution of changes in gastrointestinal motility to the pathogenesis of obesity remains controversial.3

The gold standard for measurement of gastric emptying is the scintigraphic imaging of a radiolabelled meal.4 The radiation exposure renders this test less suitable for use in children, but the gastric emptying breath test is a well-validated alternative method, which does not require the use of a radioactive label.5 Normal ranges of gastric emptying rate in children of various age groups have been reported.6

The gold standard for measuring gastric accommodation is the gastric barostat measurement. Although the gastric barostat can be used in children,7 and although abnormalities of proximal stomach function have been reported in pediatric dyspeptic patients, the barostat is too invasive for large-scale application in children.8 A simple, non-invasive drinking test has been proposed as a non-invasive method to estimate meal-induced accommodation, and was found to correlate with the gastric barostat measurements in adults.9,10 We previously established normal ranges for the satiety drinking test in healthy children between 5 and 15 years.11

The aim of this study was (i) to study the results of gastric emptying breath test and the satiety drinking test in dyspeptic and obese children, (ii) to study the relationship between daily mean caloric intake and satiety drinking test in dyspeptic and obese children.

Study Design

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

Subjects

Consecutive children with functional dyspepsia symptoms and children with obesity were recruited for participation in the study. Children with functional dyspepsia fulfilled the Rome III criteria. They underwent a personal history, clinical examination, routine biochemistry, barium swallow, and upper gastrointestinal endoscopy with biopsies. Exclusion criteria were esophagogastroduodenal lesions, a history of peptic ulcer or abdominal surgery, an underlying illness, and the use of any medication.

Fifteen obese children were referred to our hospital to start a hypocaloric diet and sport activities. They all underwent a careful history talking, clinical examination, and routine biochemistry. No obese child had symptoms or signs of underlying gastrointestinal disease.

Study protocol

Informed consent was obtained from each participant and the ethics committee at the University Hospital approved the protocol. On two separate days, the patients underwent an octanoic acid gastric emptying breath test and a satiety drinking test. Prior to the octanoic acid breath test and satiety drinking test, a dyspepsia questionnaire was filled out by each patient with the help of one or both parents. They were asked to score the presence and intensity (0–3, 0 = absent, 1 = mild, 2 = relevant, not interfering with daily activities, and 3 = severe, interfering with daily activities) of six different dyspeptic symptoms (epigastric pain, postprandial fullness, early satiety, belching, nausea, and vomiting). A 3-day nutrient history was assessed by history to calculate the mean intake daily calorie and its protein, carbohydrate, and fat content.

Satiety drinking test

Children were studied in the morning after an overnight fast. A peristaltic pump filled one of two beakers at a rate of 15 mL min−1 with a liquid meal at a constant temperature (15 °C), (Nutridrink 200 mL, 300 kcal, 13% proteins, 48% carbohydrates and 39% lipids; Nuticia, Bornem, Belgium). The children were instructed to maintain intake at the filling rate and thereby alternating the beakers by filling and drinking and scored every 5 min their satiety, graded 0–5 (1 = threshold, 5 = maximum). Children were asked to cease the study when a score of 5 was reached.

Octanoic acid breath test

The 13C octanoic breath test is a non-invasive method for measuring gastric emptying. Octanoic acid, mixed in a pancake and marked with the stable isotope 13C is immediately absorbed from the duodenum, and metabolized to 13CO2. The fraction of 13C expired in the breath indicates the rate of gastric emptying. After feeding, breath samples were collected every 15 min during 4 h. Analysis of the expired 13C fraction in the breath samples was performed using isotope-ratio mass spectrometry (Gilson ABCA 20-20 stable isotope analyser and autosampler; Europa Scientific, Crewe UK).6

Data and statistical analysis

The BMI was calculated as weight in kilogram divided by height in square meters. Gastric emptying was calculated from 13C content in the breath samples.6 The caloric intake was calculated using a dedicated software program (Becel Institute Software Nutrition, Trees Peersman, Brussels, Belgium). The results were compared to the previously established normal ranges for both tests.6,11

Data were expressed as mean ± SEM. Correlations between the endpoint of the satiety drinking test with BMI, weight, height, and age were analyzed using Pearson’s correlation analysis. Differences were compared using student’s F test or Mann–Whitney U test, and were considered to be significant at the 5% level.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

Patient characteristics

Twenty-eight dyspeptic pediatric patients (22 girls, mean age 12.5 ± 3.1 years, range 6.0–16.5 years) were recruited. The mean length, weight, and BMI were 150.8 ± 17.5 cm, 37.0 ± 11.2 kg and 15.8 ± 2.1 kg m−2, respectively (Table 1). Weight loss was reported by 8/28 patients, with a mean loss of 3.3 kg. Routine laboratory tests, screening for celiac sprue or inflammatory bowel disease, upper gastrointestinal endoscopy, and biopsies for Helicobacter pylori status were normal in all patients. Anorexia nervosa or other relevant major psychopathology was ruled out by a child psychiatrist’s assessment.

Table 1.   demographic characteristics and endpoints of satiety drinking test and gastric emptying in dyspeptic and obese children
 Dyspeptic*Obese**P (*–**)
  1. BMI, body mass index; NS, not significant.

n2815NS
Age (years)12.5 ± 3.113.3 ± 1.8NS
BMI (kg m−2)15.8 ± 2.130.0 ± 5.9<0.0001
Gastric emptying (T1/2, min)89.7 ± 54.872.5 ± 26.00.01
Satiety drinking test (mL)252 ± 85479 ± 199<0.001
Intake (cal)1503 ± 2722325 ± 469<0.0001

The most prevalent dyspeptic symptoms were early satiety (96.4%), postprandial fullness (89.2%), and epigastric pain (78.6%), followed by nausea (50%). Vomiting was present in only five children, and two children reported symptoms of troublesome belching as well.

Fifteen obese patients (five girls, mean age 13.3 ± 1.8 years, range 8.6–16.9 years) were also recruited. They had a mean body weight, length, and BMI of 85.1 ± 22.9 kg, 167.0 ± 12.4 cm, and 30.0 ± 5.9 kg m−2, respectively (Table 1). None of the obese children reported symptoms or a history of disease, nor were they taking any medication with influence on the gastrointestinal motility or secretion.

Octanoic acid gastric emptying breath test in dyspeptic and obese children

Gastric emptying test result was available for 23 of 28 dyspeptic children and 11 of 15 obese children. In dyspeptic children, the mean solid half emptying time was 89.7 ± 54.8 min (Table 1). The emptying rate was significantly delayed in six children (26%). In obese children, the mean gastric emptying rate was 72.5.0 ± 26.0 min, and all values were within the normal range (Fig. 1). As a group, dyspeptic children had significantly slower gastric emptying than that in obese children (= 0.05).

image

Figure 1.  Relationship between age and solid gastric half emptying times in children with obesity and children with functional dyspepsia. The dotted line represents the normal range determined in a previous study.6

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Satiety drinking test in dyspeptic and obese children

All dyspeptic and obese children (= 43) started the satiety drinking test and 41 children completed the test when a score of five was reached. Two children stopped prematurely because they disliked the taste of the Nutridrink test meal. The mean of the maximum ingested volume in the dyspeptic group was 252 ± 85 mL compared to 479 ± 199 mL in the obese group. Dyspeptic children ingested significantly less calories than obese children (< 0.001) or age-matched healthy children (359 ± 29 mL, = 0.001) (Table 1). The endpoint of the satiety drinking test was below the age-dependent normal range in 26/28 dyspeptic children (93%) who performed the test as indicated. The endpoint of the drinking test was abnormal in 13/15 obese children (87%) who performed the test as indicated, but their values were equally divided above and below the age-dependent normal range (Fig. 2).

image

Figure 2.  Relationship between age and amount of food ingested during a satiety drinking test in children with obesity and children with functional dyspepsia. The shaded area represents the normal range determined in a previous study.10

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Symptom scores during the satiety drinking test were significantly higher in dyspeptic children compared to health and obese, and in obese children compared to health (anova, < 0.05; Fig. 3).

image

Figure 3.  Satiety scores during a slow caloric drinking test in healthy children (from ref. Hoffman), children with obesity and children with functional dyspepsia. Satiety scores were significantly higher in children with FD (anova, < 0.05) and significantly lower in obese children (anova, < 0.05). *< 0.05 compared to healthy children; < 0.1 compared to healthy children.

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Caloric intake in dyspeptic and obese children

The caloric intake as calculated from dietary history was 1503 ± 272 cal with 13.7 ± 2.3% protein, 48 ± 7.7% carbohydrates and 39.5 ± 7.2% fat for the dyspeptic children. In the obese group the mean intake was 2325 ± 469 cal with 13.0 ± 3.0% protein, 49.2 ± 7.3% carbohydrates and 38.0 ± 5.5% fat. Obese children ingested significantly more calories than dyspeptic children (< 0.001), but the distribution of calories did not differ significantly.

A significant correlation was found between body weight or BMI and the endpoint of the satiety drinking test (both R = 0.41, = 0.04). None of the other correlations were significant.

Sweet and volume eaters in obese children

In the obese group according to the eating pattern, the patients were divided into sweet and volume eaters. Ten patients were defined as sweet eaters and five as volume eaters. The mean age, length, weight, and BMI were 12.9 ± 2.0 vs 14.0 ± 2.0 years (NS), 165.2 ± 13.9 vs 170.9 ± 8.8 cm (NS), 78.6 ± 17.0 vs 99.9 ± 28.2 kg (NS), and 29 ± 4.2 vs 34.0 ± 7.7 kg m−2 (NS), respectively. The mean gastric emptying was 66 ± 13.6 in sweet eaters compared to 83.8 ± 40.2 min in volume eaters (< 0.05), the mean of the maximum ingested volume in both groups was 475 ± 212 and 488 ± 198.4 mL (NS), respectively.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

Abnormalities of gastric motor function, in particular delayed gastric emptying and impaired gastric accommodation, have been implicated in the pathogenesis of dyspeptic symptoms, both in adults and in children.12–14 Understanding of the relationship between disordered gastric motility and dyspeptic symptoms in children has been hampered by the limitations of using tests like radioscintigraphy and gastric barostat testing. Publications have established normal values for the stable non-radioactive isotope gastric emptying breath test and nutrient drinking tests in healthy children.6,11,15 In the Sood study, a rapid drinking test was used, as children had to drink water as much as possible in 3 min and a correlation was found with age, weight, and length. This study was designed in a competitive way, with fasting during 2.5 h. Possibly due to the absence of feedback inhibition (drinking water), rapid gastric emptying may have an influence that eliminates actual filling of the proximal stomach. In adults, rapid drinking tests do not correlate well with gastric accommodation measured on a separate day with the barostat.16 Therefore, in the present study, we evaluated the use of a slow nutrient drinking test (isocaloric liquid) to evaluate gastric motor function in consecutive functional dyspepsia patients seen at a pediatric tertiary care department.

Similar to observations in adult FD,13,17,18 we confirmed that FD pediatric patients have slower gastric emptying as a group, but only a small subgroup have a gastric emptying rate that is outside of the normal range. The relevance of delayed emptying to the symptom pattern in childhood FD remains unexplored.8 In keeping with previous observations in adult functional dyspepsia,14,16,19 we observed a significantly decreased nutrient drinking capacity in children with FD. The pathophysiological correlate of decreased nutrient drinking capacity in adult FD is controversial. Impaired accommodation has been proposed as a contributing mechanism, but has not been confirmed by all groups.10,14,16,20 Although impaired accommodation is also present in a subset of childhood FD patients,8 it is not clear whether or not this is the mechanism ,which underlies decreased nutrient drinking capacity in the present study. Furthermore, we confirmed that the majority of FD pediatric patients had a nutrient drinking capacity below the lower limit of normal. Similar observations in adult FD have led to the suggestion that a drinking test could be used as a diagnostic test in adult FD.21,22 However, the present study identified a number of problems related to the use of this test in childhood FD. First of all, two children did not carry out the drink test procedure as planned, because of dislike of the taste of the nutrient mixture used in the present study. Second, the observations in obesity, as outlined below, indicate that findings of decreased nutrient drink tolerance are not limited to FD in children. In the study with dyspeptic and obese children we did not find a significant difference in the maximum tolerated volume and gender, weight, or BMI; this in contrast to the Sood study but the study population were healthy children.

The contribution of changes in gastrointestinal motility to the pathogenesis of obesity is not clear and controversial. Studies evaluating gastric capacity in obese patients using intragastric balloons or SPECT imaging have yielded conflicting results.23–25 Studies that measured gastric emptying in obese subject have reported rapid gastric emptying,26 normal emptying,27–30 or even slower emptying rates.31,32 Although better understanding of the abnormalities ,which contribute to obesity in growing children is crucial, studies in children are scarce. Most likely, obesity is a multifactorial disorder, resulting from a combination of genetic, developmental, environmental, and psychological influences. In the present small study, we observed no altered solid gastric emptying rate in obesity compared to healthy children. In adults, Kim et al., found no significant differences between asymptomatic obese and healthy subjects using the satiety drinking test.25 In the present study, we did not find a difference for the endpoint of a satiety drinking test between healthy children and childhood obesity as a group. However, there was major heterogeneity in the obese group and, whereas some drank less than the lower range of normal, a subgroup of the obese children drank more than the upper limit of normal. It is not clear whether these differences reflect heterogeneity in the pathophysiological mechanism, which leads to obesity, or whether palatability of the meal or psychological factors are confounding factors in the use of the nutrient challenge test in childhood FD. According to an analysis of daily calorie intake, the obese children in the present study ingest significantly more calories per day than the FD patients, and we did confirm a significant correlation between maximum tolerated nutrient volume and body weight. It remains conceivable that a subgroup of obese children have enhanced gastric volume capacity or decreased gastric sensitivity, allowing them to ingest larger meal volumes and to gain weight. We found no correlation between the amount of food ingested and the type of obesity as determined from dietary assessment (volume eater or sweet eater), indicating that history taking is insufficient to elucidate whether nutrient volume tolerance is enhanced or not.

In conclusion, the satiety drinking test is a potentially useful non-invasive tool in the investigation of children with FD. Further studies will be required to assess the underlying mechanism, diagnostic utility, and response to therapy of the slow nutrient drinking test. Childhood obesity is probably a multifactorial problem, and the nutrient challenge test did not give a uniformly abnormal result in this group of patients. It remains unclear whether or not increased tolerance of a nutrient challenge, present in a subset of the patients, is a relevant mechanism in the pathophysiology of childhood obesity, and further studies exploring its use and relevance seem warranted.

Acknowledgments and Disclosure

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References

No acknowledgments and disclosures. The authors have no competing interests.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Design
  5. Results
  6. Discussion
  7. Acknowledgments and Disclosure
  8. Financial Disclosure
  9. Conflict of Interest
  10. References