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Role of Nitric Oxide in the Gastric Accommodation Reflex and in Meal

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Role of Nitric Oxide in the Gastric Accommodation Reflex and in Meal 219 MOTILITY AND VISCERAL SENSATION Role of nitric oxide in the gastric accommodation reflex Gut: first published as 10.1136/gut.51.2.219 on 1 August 2002. Downloaded from and in meal induced satiety in humans J Tack, I Demedts, A Meulemans, J Schuurkes, J Janssens ............................................................................................................................. Gut 2002;51:219–224 Aims: In humans, impaired gastric accommodation is associated with early satiety and weight loss. In See end of article for animals, accommodation involves activation of gastric nitrergic neurones. Our aim was to study authors’ affiliations involvement of nitric oxide in gastric accommodation and in meal induced satiety in humans. G ....................... Methods: The effect of N -monomethyl-L-arginine (L-NMMA) 4 mg/kg/h and 8 mg/kg/h on gastric Correspondence to: compliance, on sensitivity to distension, and on gastric accommodation was studied with a barostat in Dr J Tack, Department of double blind, randomised, placebo controlled studies. The effect of L-NMMA 8 mg/kg/h on meal Internal Medicine, Division induced satiety was studied using a drinking test. of Gastroenterology, Results: L-NMMA had no significant effect on fasting compliance and sensitivity. Ingestion of a meal University Hospital induced a relaxation of 274 (15) ml which was significantly smaller after L-NMMA 4 mg/kg/h (132 Gasthuisberg, Herestraat 49, B-3000 Leuven, (45) ml; p=0.03) or L-NMMA 8 mg/kg/h (82 (72) ml; p=0.03). L-NMMA 8 mg/kg/h significantly Belgium; decreased the amount of food ingested at maximum satiety from 1058 (67) to 892 (73) kcal (p<0.01). [email protected] Conclusion: In humans, fasting gastric tone and sensitivity to distension are not influenced by nitric Accepted for publication oxide synthase inhibition, but the gastric accommodation reflex involves activation of nitrergic 6 November 2001 neurones. Inhibition of nitric oxide synthase impairs accommodation and enhances meal induced ....................... satiety. ccommodation of the stomach to a meal consists of MATERIALS AND METHODS relaxation of the proximal stomach, providing the meal Study subjects Awith a reservoir and enabling a volume increase without Twenty five healthy volunteers (16 males, aged 20–29 years) a rise in pressure. The accommodation response is mediated gave informed consent for participation in the study. None of via a vagovagal reflex pathway which activates intrinsic non- the subjects had symptoms or a history of gastrointestinal 1 adrenergic non-cholinergic neurones in the gastric wall. Sev- disease or drug allergies, nor were they taking any medication. http://gut.bmj.com/ eral lines of evidence suggest a role for both nitric oxide (NO) Informed consent was obtained from each participant. The and vasoactive intestinal polypeptide (VIP) as inhibitory neu- protocol was previously approved by the ethics committee of 2–12 rotransmitters mediating gastric relaxation. In in vivo stud- the University Hospital. ies in animals, gastric accommodation is significantly inhib- ited by NO synthase inhibitors.10–12 In humans also, ingestion Barostat study technique of a meal is accompanied by relaxation of the proximal stom- Following an overnight fast of at least 12 hours, a double ach but it is not known whether the accommodation reflex in lumen polyvinyl tube (Salem sump tube 14 Ch; Sherwood humans is mediated via activation of nitrergic neurones. Medical, Petit Rechain, Belgium) with an adherent plastic bag on October 2, 2021 by guest. Protected copyright. During fasting, gastric fundic tone in animals and humans (1200 ml capacity; 17 cm maximal diameter), finely folded, 13 14 is maintained by a vagally mediated cholinergic input. was introduced through the mouth and secured to the Recently, we demonstrated in cats that fasting fundic tone is 15 subject’s chin with adhesive tape. The position of the bag in also dependent on continuous nitrergic input. Thus fasting the gastric fundic was checked fluoroscopically. gastric tone may depend on a balance of cholinergic and The polyvinyl tube was then connected to a computer nitrergic input. It is not known whether fasting gastric fundic driven programmable volume displacement barostat device tone in humans is also under a continuous nitrergic drive. (Synectics Visceral Stimulator, Stockholm, Sweden). To unfold Functional dyspepsia is a clinical syndrome defined by the intragastric bag it was inflated with a fixed volume of 500 chronic or recurrent upper abdominal symptoms without an 16 ml of air for two minutes with the study subject in a identifiable cause by conventional diagnostic means. Several recumbent position, and then deflated completely. After a 10 studies have demonstrated impaired accommodation in func- 17–20 minute equilibration period, the subjects were positioned in a tional dyspepsia patients as a group. We reported that comfortable sitting position with the knees slightly bent (80°) accommodation is impaired in a subset of dyspeptic patients, in a bed specifically designed for that purpose. After 30 and this was associated with symptoms of early satiety and 20 minutes for adaptation, intrabag pressure was increased by weight loss. It is not known whether meal induced satiety is 1 mm Hg every one minute to determine minimal intragastric under nitrergic control in humans, and whether pharmaco- distending pressure (MDP) as the lowest pressure level that logically induced impairment of gastric accommodation provided an intrabag volume of 30 ml or more.23 This pressure would be accompanied by early satiety in healthy subjects. G level equilibrates intra-abdominal pressure. N -monomethyl-L-arginine (L-NMMA) is an inhibitor of Throughout all studies, systolic and diastolic blood pres- NO synthase, suitable for use in humans. Recent studies using sures were measured at 10 minute intervals. this agent have demonstrated involvement of NO in the con- trol of interdigestive motility and in transient lower oesopha- geal sphincter relaxation in humans.21 22 We used these ............................................................. properties to test the hypothesis that NO is involved in the Abbreviations: MDP, minimal distending pressure; L-NMMA, G control of fasting and postprandial gastric tone and of meal N -monomethyl-L-arginine; NO, nitric oxide; VIP, vasoactive intestinal induced satiety in humans. polypeptide; 5-HT, 5-hydroxytryptamine. www.gutjnl.com 220 Tack, Demedts, Meulemans, et al Influence of L-NMMA on fasting gastric tone and on the To evaluate the effect of L-NMMA on gastric compliance and perception of gastric distensions perception of gastric distension, the mean responses to the Seven healthy subjects (five males) underwent a gastric baro- same pressures applied before and after drug administration, stat examination three times, with an interval of one week. as well as the intercepts and slopes obtained by linear Gut: first published as 10.1136/gut.51.2.219 on 1 August 2002. Downloaded from Graded isobaric distensions were performed in stepwise regression analysis of pressure-volume curves and distension- increments of 2 mm Hg starting from MDP, each lasting for perception curves, were compared by Student’s t test. The two minutes, while the corresponding intragastric volume was number of subjects that reported perception or discomfort at a recorded. Subjects were instructed to score their perception of given distending pressure were compared before and after upper abdominal sensations at the end of every distending drug administration using a logistic regression procedure with step, using a graphic rating scale that combined verbal stratification, implying exact conditional inference. In addi- descriptors on a scale graded from 0 to 6.23 The end point of tion, the perception and discomfort thresholds before and each sequence of distensions was established at an intrabag after L-NMMA were compared using the paired Student’s t volume of 1000 ml or when subjects reported discomfort or test. pain (score 5 or 6). Subsequently, the pressure level was set at Meal induced gastric relaxation was quantified by calculat- MDP+2 mm Hg for 30 minutes. Thereafter graded distensions ing the difference between the average intragastric volume for were repeated. Twenty minutes prior to the second set of dis- the 30 minutes before and the first 45 minutes after adminis- tensions, placebo, L-NMMA 4 mg/kg/h, or L-NMMA 8 mg/kg/h tration of the meal. Also, the amplitude of the maximal was administered in a double blind, randomised, crossover relaxation was calculated as the difference between the aver- fashion via continuous intravenous infusion over 45 minutes. age preprandial volume and the highest postprandial five minute interval mean volume, and the time needed to reach Influence of L-NMMA on gastric accommodation to a the maximum postprandial volume was calculated. The meal amplitude of the relaxations after placebo and L-NMMA were Seven different healthy subjects (five males) underwent a compared using the Student’s t test. In addition, analysis of gastric barostat examination three times, with an interval of covariance was performed on postprandial intraballoon one week. The pressure level was set at MDP+2 mm Hg for at volumes with pre-meal volume as a covariate. least 90 minutes. After 30 minutes, a liquid meal (200 ml, 300 For meal induced satiety testing, the average satiety score at kcal, 13% proteins, 48% carbohydrates, 39%; Nutridrink, the end of infusion of placebo or L-NMMA (60 minutes after Nutricia, Bornem, Belgium) was administered. Twenty min- the start of the meal) was determined and the amount of utes prior to the meal, placebo, L-NMMA 4 mg/kg/h, or calories ingested until the occurrence of maximum satiety L-NMMA 8 mg/kg/h was administered in a double blind, ran- (score of 5) was calculated. Differences were considered to be domised, crossover fashion via continuous intravenous infus- significant at the 5% level. ion over 60 minutes. RESULTS Satiety testing Conduct of the study Eleven healthy subjects (six males) participated in meal All participants completed the studies as planned.
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