Altered solid and liquid gastric emptying in patients

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1 Gut, 1985, 26, Altered solid and liquid gastric emptying in patients with duodenal ulcer disease G J MADDERN, M HOROWITZ, D J HETZEL, AND G G JAMIESON From the Departments ofsurgery, Medicine, and Gastroenterology, University ofadelaide, Royal Adelaide Hospital, Adelaide, South Australia SUMMARY Alteration in gastric emptying has been implicated in duodenal ulcer disease. The precise abnormalities remain controversial. We have used a radionuclide technique to assess solid and liquid gastric emptying in 14 patients with endoscopically proven duodenal ulcer and 22 healthy controls. Solid gastric emptying values for the patient group fell within the normal range. The median time taken for 5% (T5) of the liquid marker to empty from the stomach was 12 minutes (range 6-23 minutes) which was significantly faster (p< 5) than controls (median 18 minutes, range 11-35). In 1 of the 14 patients, however, the rate of liquid emptying was within the normal range. There was no significant difference in the T5 for gastric emptying of solids between the groups, but in duodenal ulcer patients food left the stomach significantly earlier than in controls (p<.5). After this, however, the linear rate at which duodenal ulcer patients emptied solid food from the stomach was a median -75%/minutes (range minutes), which was slower (p<.5) than controls, median 1-25/minutes (range.7-2.3). These results show that the pattern of gastric emptying of digestible solids and liquids in patients with duodenal ulcer disease, as a group, is significantly altered. The role played by gastric emptying in duodenal ulcer disease is unclear. ' The results of studies which have assessed emptying of meals have been conflicting.2-7 This has probably occurred because of the complexity and variability of the composition of the meals used and also because intubation techniques can interfere with normal physiological function.8 We have used an improved radionuclide technique9 in an attempt to avoid these problems to assess solid and liquid emptying in both healthy controls and patients with duodenal ulcer disease. Subjects Twenty two normal healthy volunteers (12 men, 1 women) median age 34 years (range years) and 14 patients (13 men, one woman) median age 53-5 years (33-66 years) with duodenal ulcer were studied after giving informed consent for the study. All controls were free of symptoms, had no past history of upper gastrointestinal disease, were nonsmokers and were not taking medications. The 14 Address for correspondence: Professor G G Jamieson, Department of Surgery, Royal Adelaide Hospital, Adelaide, South Australia 5. Received for publication 1 September 1984 duodenal ulcer patients all had an endoscopically confirmed duodenal ulcer before the investigation, and none had clinical or endoscopic evidence of pyloric stenosis. Ten smoked between 5-4 cigarettes per day, the remaining four being reformed smokers. No patient received medication for 48 hours before the investigation. Radionuclide assessment: the gastric emptying test was carried out after an overnisght fast. The method has been reported previously.' While eating a standard solid and liquid meal, the subject sat in front of a scintillation camera, with the camera to the subject's back. The solid component of the meal was a 1 g 'hamburger' of ground beef incorporating 1-2 mci of 99mTc-sulphur colloid tagged to chicken liver.1 The liquid marker was *5-1- mci of ll3min DTPA mixed in 15 ml of 1% dextrose. The scintillation camera was interfaced to a computer for data collection. The energy window alternated regularly between that of ll3min (393 kev) and 99mTc (14 kev) using an automatic switching device. Data were collected for 12 minutes. At the end of data acquisition, 1,uCi of 99mTc-DTPA in 15 ml of water was given orally and a one-minute left lateral image of the upper abdo- 689 Gut: first published as /gut on 1 July Downloaded from on 17 September 218 by guest. Protected by copyright.

2 69) men was taken to allow for attenuation correction. 12 The computer data comprised list mode files which were reformated to produce separate dynamic studies for the solid and liquid components. Corrections were made for '33mIn-Compton scatter, attenuation, patient movement and radionuclide decay. Analysis of the data by use of computer drawn regions-of-interest that included the stomach but excluded the intestine enabled calculations to be made of the time for 5% of the liquid tracer to leave the gastric region (Liquid T5). Solid emptying characteristics were assessed by considering the time taken from ingestion until solid began to leave the stomach (lag period), time taken for 5% to leave the stomach (solid T5) and the percentage of the marker remaining at 1 minutes. The rate at which the solid component of the meal emptied as a percentage per minute was also calculated. STATISTICAL ANALYSIS Data were analysed using the Wilcoxon's unpaired test. Results SOLID EMPTYING In all subjects solid emptying was slower than liquid emptying and was characterised by a lag period followed by linear emptying (Fig. 1). There was no significant difference (Table) for the solid T5 between the controls and patient groups. All patients fell within the normal range (Fig. 2). Both the lag period and the linear emptying rate, howev-.o c 4, (a) Solid J Postcibal minutes Maddern, Horowitz, Hetzel, and Jamieson Table Results of gastric emptying in controls and patients with duodenal ulcers. Control Duodenal Significance ulcer level Subjects (no) Solid lag period (min) p<(5 (9-69) (1-32) Solid linear rate (%/min) 1 25 (75 P< 5 (-7-2-3) (-5-1.4) Solid T5 (min) ns (5-122) (54-113) Solid retention at It)) min (%) 3) 42 ns (12-65) (16-6) LiquidT5((min) p< J)5 (11-35) (6-23) Data are median values with range in parentheses. er, were significantly altered in the patient group (Table). LIQUID EMPTYING The liquid emptying was non-linear and followed a mono-exponential pattern (Fig. 1). Liquid T5 was significantly faster (Table) in the patient group than the controls. Four of the patients had a liquid T5 faster than the normal range (Fig. 3). Discussion Our study confirms the findings of others using intubation techniques that duodenal ulcer patients empty liquids more rapidly than normal indi- 2- (b) -Lquid 1. \ ~~~Control O * Duodenal o--... I uicer patient m Postcibal minutes 8 1 Fig. 1 Solid and liquid gastric emptying curves for controls and patients with duodenal ulcer. Values are mean ±SEM. Gut: first published as /gut on 1 July Downloaded from on 17 September 218 by guest. Protected by copyright.

3 Altered solid (11t(d liql(id gastric emptyving in patienits withi dutodenal uilcer disease 12 1 T5 for solid 8 emptying (min) ' T5 for liquid ernptying (min) 15' S OS I ± L C. t.". Controls viduals3 "' although the 5% emptying time was outside the normal range in only four patients. A I non-invasive radionuclide study, however,'- failed to show any significant difference between five duodenal ulcer patients and five controls for solid * and liquid emptying; this may have been because of the small number of patients studied. The technique used in that study was similar to our own methods except that a different meal was used (cornflakes, sugar and milk, with indigestible paper pieces impregnated with 99"llTc sulphur colloid as a solid phase marker) and scans were undertaken in the supine position. No corrections were made for attenuation of activity in the gastric region of interest and therefore only gross differences were likely to be found, particularly in liquid emptying. Controls Duodenal Most reports of studies using a mixing solid and ulcer patients liquid nileal have used intubation techniques. Those Fig. 2 Individual solid gastric emptying resuilts e.xpressed studies which have considered solid emptying have as time taken for 5% of meal to clear the gas. tric region reported more rapid emptying13 14 or no change (T5) for controls and patients with duodenall ulcer. The from normal.4 12 These discrepancies may relate to line dividing each group represents the media, n value. 5- the different methods used or depend on the ph or caloric content of the meal, since increases in duodenal acidity and large caloric intakes cause less slowing of gastric emptying in duodenal ulcer patients than control subjects.8 13 Howlett et a14 found that the T5 for solids was similar in both duodenal ulcer patients and a control group. By use of component analysis, however, they showed that the pattern of emptying was different. We found also that there was no difference from controls in T5 for solids in duodenal ulcer patients * although solid emptying started earlier and the rate of emptying was slower in our patient group * compared with our control group. There are several possible explanations for our * findings. The age of our patient group was older * than that of our controls (53.5 vs 34). An age * difference of this magnitude, however, is most so unlikely to affect the results of gastric emptying studies.'5 16 Pylorospasm and pyloric stenosis were - unlikely to be significant factors as there was no _w evidence of either problem in the investigation of the patients and such hold up would have tended to * slow gastric emptying of liquids rather than accelerate it. We have not found any significant difference in gastric emptying between men and women in our control studies and so the different sex ratio between our groups is unlikely to have been a factor Duodenal in the differences observed. ulcer patients Smoking immediately before performance of a gastric emptying test has been shown to accelerate Fig. 3 Individual liquid gastric emptying re. sults expressed li 17 as the time taken for 5% of the liquid meal tfo clear the lquid gastric emptying and so our patients rewithlduodenal frained from smoking on the day of their study. All gastric region (T5) for controls and patients,-with ulcer. The line dividing each group represents the median 14 patients had been smokers, although four had value. reformed. We were not able to show any significant 691 Gut: first published as /gut on 1 July Downloaded from on 17 September 218 by guest. Protected by copyright.

4 692 Maddern, Horowitz, Hetzel, and Jamieson correlation between the number of cigarettes smoked per day and the rate of liquid emptying. Further it has been shown'7 that non-smokers do not differ significantly from smokers in their emptying of liquids. It would appear that any role played by cigarette smoking is an immediate one, but its mechanism remains unclear. A deficiency of all radionuclide methods is that gastric emptying of the solid and liquid marker is measured and the effects of dilution by gastric secretion cannot be quantified. Although differences in gastric secretion rates between the control subjects and duodenal ulcer patients could theoretically have influenced the results, this appears very unlikely. Differences in gastric secretion between duodenal ulcer patients and normal subjects do not occur until 4 minutes after ingestion of a meal of neutral ph.7 The meal given to our patients was of neutral ph and differences in the rate of both liquid and solid emptying were observed before 4 minutes in most patients. In addition, dilution by gastric secretion would probably produce a tendency for delayed, rather than the observed more rapid gastric emptying in the DU patients. The duodenum has ph sensitive receptors which regulate gastric emptying in normal subjects, probably by a hormonal mechanism These receptors act to keep the duodenal milieu at around a ph of 6.11 Read et a18 found that duodenal ulcer patients appear to have an impairment of their capacity to slow gastric emptying in response to an increasing load of acid in the duodenum. Such impairment might explain why liquid emptying was more rapid in our patients and one implication is that an acid load also enters the duodenum more rapidly in these patients. The rapid emptying does not appear to be related to acid hypersecretion, as many patients with normal acid output have increased fractional emptying rates.2 Antral dysfunction has been recorded in association with delayed solid gastric emptying21 and this is a possible explanation for the changes in solid gastric emptying which we observed. Our findings support the hypothesis that there is dysfunction of the duodenal receptors which regulate gastric emptying, in patients with duodenal ulcer disease. The mechanism of such dysfunction, however, remains poorly understood. The place of rapid gastric emptying of liquids as a cause of duodenal ulcer remains uncertain, and the alterations we have described may be a consequence rather than the cause of the ulcer. Dr Maddern was supported by a grant from the E R Dawes, L C Hughes, A R Curren Research Fellowships; Dr M Horowitz was supported by a grant from the National Health and Medical Research Council of Australia. References 1 Wormsley KG. The pathophysiology of duodenal ulceration. Gut 1974; 15: Hunt JN. Inhibition of gastric emptying and secretion in patients with duodenal ulcer. Lancet 1957; 1: Bromster D. Gastric emptying rate in gastric and duodenal ulceration. Scand J Gastroenterol 1969; 4: Howlett PJ, Sheiner HJ, Barber DC, Ward AS, Perez-Avilla CA, Duthie HL. Gastric emptying in control subjects and patients with duodenal ulcer before and after vagotomy. Gut, 1976; 17: Malagelada J-R, Longstreth GF, Derring TB, Summerskill WHJ, Go VLW. Gastric secretion and emptying after ordinary meals in duodenal ulcer. Gastroenterology 1977; 73: Wormsley KC. Response to duodenal acidification in man. IV. Effect on gastric emptying. Scand J Gastroenterol 1972; 7: Lam SK, Isenberg JI, Grossman MI, Lane WH, Hogan DL. Rapid gastric emptying in duodenal ulcer patients. Dig Dis Sci 1982; 7: Read NW, Al Janabi MN, Bates TE, Barber DC. Effect of gastrointestinal intubation on the passage of a solid meal through the stomach and small intestine in humans. Gastroenterology 1983; 84: Collins PJ, Horowitz M, Cook DJ, Harding PE, Shearman DJC. Gastric emptying in normal subjects, a reproducible technique using a single scintillation camera and computer system. Gut 1983; 24: Meyer JH, Macgregor IC, Gueller R, Martin P, Cavalieri R. 99mTc-tagged chicken liver as a marker df solid food in the human stomach. Dig Dis Sci 1976; 21: Hunt JN, Knox MT. The slowing of gastric emptying by four strong acids and three weak acids. J Physiol (Lond) 1972; 222: Heading RC, Tothill P, McLoughlin GP, Shearman DJC. Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components of a meal. Gastroenterology 1976; 71: Stubbs DF, Hunt JN. A relation between the energy of food and gastric emptying in men with duodenal ulcer. Gut 1975; 16: Griffith GH, Owen GM, Campbell H, Shields R. Gastric emptying in health and gastroduodenal disease. Gastroenterology 1968; 54: Horowitz M, Maddern GJ, Chatterton BE, Collins PJ, Harding PE, Shearman DJC. Gastric emptying in the elderly. Clin Sci 1984; 67: Moore JC, Tweedy C, Christian PE, Data FL. Effect of Gut: first published as /gut on 1 July Downloaded from on 17 September 218 by guest. Protected by copyright.

5 Altered solid and liquid gastric emptying in patients with duodenal ulcer disease 693 age on gastric emptying of liquid-solid meals in man. Dig Dis Sci 1983; 28: Grimes DS, Goddard J. Effect of cigarette smoking on gastric emptying. Br Med J 1978; 2: Strunz E. Hormonal control of gastric emptying. Acta Hepato-Gastroenterol 1979; 26: Dalton MD, Eisenstein AM, Walsh JH, Fordtran JS. Effect of secretin on gastric function in normal subjects and in patients with duodenal ulcer. Gastroenterology 1976; 71: Dubois A, Castell DO. Abnormal emptying response to pentagastrin in duodenal ulcer disease. Dig Dis Sci 1981; 26: Holt S, Reid J, Taylor TV, Tothill P, Heading RC. Gastric emptying of solids in man. Gut 1982; 144: Gut: first published as /gut on 1 July Downloaded from on 17 September 218 by guest. Protected by copyright.

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