Received: 13 October 2021 | Revised: 2 February 2022 | Accepted: 24 February 2022 DOI: 10.1111/nmo.14351 ORIGINAL ARTICLE Effect of colonic distension on small bowel motility measured by jejunal high-­resolution manometry Luis G. Alcalá-Gonzalez1,2 | Carolina Malagelada1,2 | Dan M. Livovsky1,2 | Fernando Azpiroz1,2 1 Department of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain Abstract Background: Abnormal motility patterns in the jejunum can be detected in patients 2 Digestive System Research Unit, University Hospital Vall d'Hebron Barcelona, Centro de Investigación with prominent colonic content, and these abnormalities may be due to either a pri- Biomédica en Red de Enfermedades mary jejunal dysfunction or a reflex distortion. The objective of the present study was Hepáticas y Digestivas (Ciberehd), Barcelona, Spain to determine the effect of colonic distension on small bowel postprandial motility using high-­resolution manometry. Correspondence Carolina Malagelada, Digestive System Methods: Single center, controlled, parallel, randomized, single blind study in healthy Research Unit, University Hospital Vall subjects testing the effect of colonic filling vs sham infusion on the responses to a d'Hebron, Barcelona 08035, Spain. Email: cmalagelada@vhebron.net meal in 16 healthy subjects. Nutrients were continuously infused in the proximal je- junum (2 Kcal/min) during the 2-­h study period to induce a steady-­state postprandial Funding information Instituto de Salud Carlos III, Grant/Award motor pattern. Jejunal motility was measured by water-­perfused, high-­resolution ma- Number: CM20/00182 and PI17/01794; nometry. After 1 h postprandial recording (basal period), gas was infused during 7.5 Israeli Gastroenterological Association; Centro de Investigación Biomédica en Red min via a rectal tube (720 mL or sham infusion), and jejunal motility was recorded for de Enfermedades Hepáticas y Digestivas; another hour. Ministerio de Ciencia e Innovación, Grant/ Award Number: SAF 2016-­76648-­R; Key Results: Jejunal postprandial motility during the basal period was characterized Societat Catalana de Digestologia by two overlapping components: a) continuous segmental activity (non-­propagated or shortly propagated) and b) intercurrent propagated fronts (3.8 ± 1.1 fronts of 2-­5 clustered contractions/h >10 cm propagation). As compared to sham infusion, colonic gas filling: a) inhibited continuous segmental contractile activity (by 17 ± 4%; p = 0.044 vs control group) and b) stimulated intermittent propagated fronts (up to 9.0 ± 2.2 fronts/h; p = 0.017 vs control group). Conclusions and Inferences: Long retrograde reflexes induced by colonic distension distort the balance between segmental and propagated activity, and may affect the normal response of the jejunum to food ingestion. Jejunal manometry in patients may be artifacted by colonic overload. KEYWORDS colonic distension, high-­resolution manometry, postprandial motility, propagated contractions, small bowel motility This is an open access article under the terms of the Creative Commons Attribution-­NonCommercial-­NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-­commercial and no modifications or adaptations are made. © 2022 The Authors. Neurogastroenterology & Motility published by John Wiley & Sons Ltd. Neurogastroenterology & Motility. 2022;00:e14351.  wileyonlinelibrary.com/journal/nmo | 1 of 8 https://doi.org/10.1111/nmo.14351 2 of 8 | ALCALÁ et al. 1 | I NTRO D U C TI O N sensations, abdominal girth, and vagal tone (Figure 1). Randomization into test group (with rectal gas infusion) and control group (sham in- Intestinal manometry is the current gold standard for the evaluation of fusion) was performed 1:1 by a computer-­generated list. The study patients with suspected small bowel dysmotility.1 However, patients protocol was approved by the Ethics Committee of the University with suspected dysmotility frequently present colonic distension, and Hospital Vall d’Hebron, and all participants gave their written informed in this case, it becomes uncertain whether manometric abnormalities consent before enrollment. The study protocol was registered with the in the small bowel are related to a primary intestinal disorder, for ex- ClinicalTrials.gov (ID: NCT05046743). All co-­authors had access to the ample, gut neuro-­myopathy, or are secondary to colonic distension, study data and reviewed and approved the final manuscript. for example, responses to long-­distance retrograde reflexes. We hypothesized that colonic distension may elicit long-­distance retrograde reflexes targeting the upper gut. Our aim was to determine 2.2 | Participants whether and in what form, colonic distension may affect small bowel motility. Since the dysmotility associated to colonic distension is more Sixteen healthy, non-­obese subjects without a history of gastroin- 2 evident during the postprandial period, we tested the effect of colonic testinal symptoms were recruited by public advertising. Exclusion distension on postprandial motility, experimentally induced by contin- criteria were chronic health conditions, use of medications (except uous infusion of nutrients directly into the small bowel. In this proof-­ sporadic use of NSAIDs and antihistaminics), alcohol abuse and of-­concept study, we tested physiologic levels of colonic distension, use of recreational drugs. Absence of current digestive symptoms using an experimental model that has been previously validated in our was verified using a standard abdominal symptom questionnaire laboratory.3–­5 The jejunal response to colonic distension was evaluated (no symptom > 2 on a 0–­10 scale). Psychological and eating dis- by means of high-­resolution manometry (HRM) with multiple, closely orders were excluded using the following tests: Hospital Anxiety spaced recording sites, because recent studies showed that HRM iden- and Depression scale (HAD), Dutch Eating Behavior Questionnaire 6 tifies motor features undetectable by conventional manometry. (DEBQ—­Emotional eating, External eating, Restrained eating), and Physical anhedonia scale (PAS). 2 | M ATE R I A L A N D M E TH O DS 2.3 | Interventions 2.1 | Study design 2.3.1 | Jejunal nutrient infusion Single-­center, controlled, parallel, randomized, single blind study in healthy subjects testing the effect of colonic distension on the re- Postprandial condition was induced using a formula composed sponses to meal ingestion. Colonic distension was produced by filling of 250 ml of a liquid nutrient mixture (Fresubin Protein Energy, the colon with gas. The primary outcome was the effect on postprandial Fresenius Kabi, 1.0 kcal/ml) combined with 85 ml of drinkable water. jejunal motility; secondary outcomes were the changes in postprandial Using an infusion pump (Compat Ella, Nestle) at a rate of 165 ml/h a F I G U R E 1 Experimental design. The responses to intestinal nutrients (outcomes) were measured before (basal) and during colonic filling; the effects of gas versus sham filling were compared in a parallel, randomized design in healthy subjects (n = 16) ALCALÁ et al. | 3 of 8 steady nutrient infusion of 2.0 Kcal/min was achieved. The nutrient pressure), (b) sensation of abdominal distension (defined as sensation infusion was infused into the jejunum via a catheter (1.02 mm inner of increase in girth), (c) borborygmi/colicky sensation, (d) abdominal diameter) attached to the manometric tube (see below). The nutri- discomfort, and (e) nausea/vomiting; scales graded from −5 to +5 ent infusion was started at the beginning of the experiment and was were used to measure: (f) hunger/satiety (from extremely hungry to maintained during the 2-­h study period. completely satiated), (g) digestive well-­being (extremely unpleasant to extremely pleasant) and (h) mood (very negative to very positive). Subjects received standard instructions on how to fill-­out the scales 2.3.2 | Colonic filling to report the sensations perceived over the preceding 15-­min period during the study (Figure 1). This method has been extensively used After 1 h jejunal nutrient infusion, a balloon-­catheter (Foley catheter and validated in detail.3,5,8 20 F; Bard, Barcelona, Spain) was introduced into the rectum and hermetically connected to a volumetric pump (BIG-­3000, Soifer). The intra-­rectal balloon was inflated with 10 ml of water to prevent 2.4.3 | Changes in girth anal gas leaks. In the test group, 720 ml of a gas mixture was in- fused into the colon over a 7.5-­min period (at a constant flow rate Once the participants were positioned in bed (see Procedure of 96 ml/min); subsequently the outflow was blocked and colonic below), a non-­ stretch belt was placed over the umbilicus. The gas filling was maintained during 1 h. The gas mixture infused (88% overlapping ends of the belts were carefully adjusted by means of nitrogen, 6.5% carbon dioxide, and 5.5% oxygen, bubbled into water two elastic bands so that the belts constantly adapted to the cir- for saturation) mimicked the partial pressures of venous blood gases cumference of the abdominal wall. Measurements during the study to minimize diffusion across the intestine–­blood barrier.7 In the con- were directly taken using a metric tape measure attached to the trol group a sham infusion was performed. At the end of the study belts.4 Measurements were taken at 15-­min intervals without ma- the rectal tube was opened to allow colonic venting (Figure 1). nipulation of the belt-­t ape assembly. 2.4 | Outcome measures 2.4.4 | Vagal tone 2.4.1 | Jejunal motor activity A subset of participants (n = 8, four patients from each group) un- derwent continuous heart rate monitoring during the study to assess Jejunal motility was measured by high-­resolution manometry, using a changes in heart rate variability. High quality inter-­beat data was re- 6 technique that has been described before in detail. In brief, a custom- corded during the entire experiment using a Bluetooth heart rate ized 35-­channel perfusion catheter (Mui Scientific) made of silicone (ex- strap (H10, Polar Electro). R-­R intervals and cardiac interbit intervals ternal diameter of 4.7 mm) was used. Perfusion side-­holes (recording were obtained. Vagal tone was assessed using the root mean square sites) were located 58 and 48 cm from the tip of the catheter, to register of the successive differences between normal heartbeats (RMSSD), antral and duodenal contractions, respectively; the following 33 side-­ as described previously.9 holes were spanned at 1-­cm intervals from 37 to 5 cm from the tip, to measure jejunal contractile activity. The nutrient perfusion tube was at- tached to the manometric tube with the distal end opening 38 cm from 2.5 | General procedure the tip, that is, 1 cm above the first jejunal recording site. After calibration of the manometric system, the catheter with Participants were instructed to follow a diet excluding legumes, a metallic guidewire in the central lumen to facilitate localization, vegetables, onion, garlic, nuts, cereals, whole meal bread and fizzy was introduced transnasally and placed into the small bowel under drinks for the 2 days prior to the study; meat, fish, eggs, rice, pasta fluoroscopic control. After intubation, participants were positioned and/or white bread were permitted, while dairy products, salad, supine in bed, and the catheter was connected to a low-­compliance fruit, and alcoholic beverages were prohibited. The evening before manometric system (Solar GI HRM, MMS-­L aborie) and each channel the study, they were instructed to eat a light dinner. was perfused with distilled water at 0.15 ml/min (total volume in- The studies were conducted in a quiet isolated room after an 8-­h fused 315 ml/h). Jejunal motility was continuously registered during fast. After intubation, participants were positioned supine in bed, the 2-­h study period. the manometric catheter was connected to the manometric system, and jejunal manometry was continuously recorded throughout the study. After a 10-­min equilibration period, jejunal nutrient infusion 2.4.2 | Digestive sensations was started and maintained until the end of the studies. The re- sponses to jejunal nutrients were measured for 1 h (basal period). Perception scales graded from 0 (not at all) to 6 (very severe) Subsequently, the balloon-­catheter was positioned into the rectum, were used to measure: (a) abdominal bloating (defined as fullness/ connected to the infusion pump and either gas (in the test group) 4 of 8 | ALCALÁ et al. TA B L E 1 Demographics sham infusion (in the control group) was performed for 7.5 min and anal outflow was blocked. The effect of colonic filling (with gas or Test group Control group p value sham) on postprandial activity was studied for 1 h (intervention pe- Female/male 3/5 3/5 0.617 riod) (Figure 1). Age, years 24.0 ± 2.7 22.5 ± 0.8 0.114 Weight, kg 69.6±4.3 69.5 ± 2.7 0.873 2 BMI, kg/m 22.5 ± 0.6 22.6 ± 0.5 0.999 2.6 | Data analysis Abbreviation: BMI, body mass index. Manometric recordings were analyzed (by CM and LA) both visu- ally and using the MMS Database Software v9.5h (MMS-­L aborie), 3 | R E S U LT S as previously described. 6 The total number of phasic pressure waves (reversible pressure increase >10 mmHg, lasting >2 s and 3.1 | Demographics and study flow <10 s) was automatically measured by computerized analysis. Propagated fronts (2–­5 contractions propagating over at least 10 Sixteen healthy subjects (6 women and 10 men, 19–­4 4 years age contiguous recording sites) were visually identified. Their velocity range, body mass index between 18.5 and 28 kg/m2) were rand- of propagation was measured as the length of propagation (dis- omized into test or control groups. There were no differences in age, tance between the first and last sensor detecting each propagated gender distribution or body mass index between groups (Table 1). event) divided by the duration of propagation (time interval be- Two participants, one in each group, did not tolerate the study pro- tween the onset of the contraction at the first and last sensor). cedure and withdrew from the study before the intervention period. Contractile activity that did not fulfill the criteria of propagated Fourteen subjects completed the study protocol (7 subjects per front [non-­p ropagated or shortly propagated (<10 cm) contrac- group) and were included for analysis. tions], that is, segmental activity, was not directly quantified, but was inferred from the total number of contractions.6 The out- comes were analyzed during the last 45 min of the basal period 3.2 | Postprandial motor activity (basal period) and the intervention period. Changes in abdominal girth during the study were refer- During the basal period, a postprandial-­t ype motility pattern was enced to the girth measurement at the beginning of the study, recorded in all subjects, characterized by two overlapping com- that is, before jejunal nutrient infusion was started. Vagal tone, ponents: a background of segmental activity (non-­propagated or measured by heart rate variability (HRV), was assessed: (a) at the shortly propagated contractions) with intercurrent propagated beginning of the experiments, (b) during the basal period, and (c) fronts (3.8 ± 1.1 fronts/h) (see definitions in Data analysis sec- during the intervention period (either gas or sham colonic filling). tion above; Figures 2 and 3). Most propagated fronts (79%) origi- Prior to HRV computation, all recorded data were visually in- nated at the proximal recording sites and propagated aborally (at spected for correctness, and then underwent automatic artifact 0.75 ± 0.3 cm/s) throughout the 33 jejunal recording sites (32 cm); correction. HRV analysis of the exported data was performed the rest originated at different levels and propagated aborally over on a computer using a dedicated HRV software (HRV Premium a mean of 28 ±1 cm (no retrograde propagation was observed). The 3.4.2, Kubios Oy). number of propagated fronts was similar in the proximal and distal recording sites; however, segmental activity was more prominent in the proximal than in the distal part of the jejunum, and this was 2.7 | Statistical analysis reflected by a higher number of total contractions (3.1 ± 0.4 vs. 2.2 ± 0.3 contractions/min, respectively; p = 0.001). No differences Primary statistical analysis was performed by comparing the effect between test and control groups were detected during the basal pe- of the intervention (differences from basal period) in the gas infusion riod (Figure 3). group (test) versus sham infusion group (control). Statistical analysis was performed with SPSS Statistics for Windows (V22.0, IBM). Data are presented as mean values ± stan- 3.3 | Effect of colonic distension on jejunal motility dard error. Normality of data distribution was evaluated by the Shapiro Wilk test. Comparisons of parametric, normally distrib- In the test group, colonic filling with gas produced a significant uted data were made by Student's t-­test, paired tests for intra- change in jejunal motility with differential effects on the two group comparisons and unpaired tests for intergroup comparisons; components of the postprandial pattern, as follows (Figures 2 otherwise, the Wilcoxon signed rank test was used for paired data and 3). Colonic filling with gas was associated with an increase in within groups, and the Mann-­W hitney U test for unpaired data the number of propagated fronts (increase by 4.1 ± 1.1 fronts/h; between groups. Differences were considered significant at a p p = 0.027 vs. basal period), without significant differences in the value < 0.05. site of origin, velocity or distance of propagation. However, the ALCALÁ et al. | 5 of 8 F I G U R E 2 Examples of jejunal high-­resolution manometry in the same subject. Note, stimulation of propagated fronts during colonic filling (B) as compared to basal (A) The effect of gas filling on jejunal motility was triggered immedi- ately after gas infusion (3.5 ± 0.4 contractions/min during the 5 min before gas infusion vs. 2.8 ± 0.5 contractions during the 5 min im- mediately after gas infusion; p < 0.05), and was maintained through- out the whole intervention period (2.2 ± 0.4, 2.3 ± 0.5, 2.2 ± 0.5 contractions/min in the first, second and third 15-­min evaluation periods during gas infusion). In the control group, sham infusion did not modify jejunal motor activity, neither the number of propagated fronts (change by 0.9 ± 0.5 propagated fronts/h; p = 0.484 vs. basal period) or total number of contractions (10 ± 11% change from basal; p = 0.537 vs basal period) nor (Figure 3). The changes from basal were signifi- cantly different between test and control groups, both the num- ber of propagated fronts (p = 0.017) and total contractile activity (p = 0.044). 3.4 | Perception of digestive sensations All subjects tolerated jejunal nutrient infusion during the basal pe- F I G U R E 3 Effect of colonic filling on postprandial small riod with perception of mild digestive sensations, similar in con- bowel motility. Continuous segmental activity [non-­propagated trol and test groups; to note, participants reported sensation of or shortly propagated (<10 cm) contractions] decreased, and intercurrent propagated (>10 cm) fronts increased during colonic digestive well-­being and positive mood. In the control group, no gas filling (test group), whereas sham infusion had no effects changes in digestive postprandial sensations were observed during (control group) sham infusion. In the test group, colonic filling with gas induced an increase in perception of digestive sensations (Figure 4), and the total number of contractions decreased (by 17 ± 4%; p = 0.033 effect (delta from basal) was significantly more prominent than vs. basal period), reflecting a reduction in segmental activity; no that of sham infusion for the sensation of abdominal distension region-­s pecific differences were detected (total number of con- (p = 0.007), fullness (p = 0.009) and discomfort (p = 0.001). These tractions decreased by 14 ± 5% in the proximal and 21 ± 7% in sensations were associated with a significant impairment of diges- the distal part; p = 0.404). tive well-­being in the test group (p = 0.006 vs. basal), but not in the 6 of 8 | ALCALÁ et al. control group; p = 0.457 vs. basal and p = 0.005 vs. test group); a RMSSD change by 2.0 ± 2.8 ms; p = 0.251 vs. basal; p = 0.185 vs. similar trend (not reaching statistical significance) was observed for gas infusion). mood (Figure 4). 4 | DISCUSSION 3.5 | Effect on abdominal girth Our data indicate that relatively mild colonic distension in healthy During the basal period, jejunal nutrient infusion did not induce girth subjects induces long-­distance retrograde reflexes affecting jejunal changes in either the test or control groups. In the test group, co- motor activity. lonic gas filling induced a significant increase in girth (by 17 ± 3 mm; In our experimental model, continuous infusion of nutrients di- p = 0.002 vs. basal), but no change was observed during sham infu- rectly into the jejunum induced a steady-­state motor activity, with- sion in the control group (change by −1 ± 2 mm; p = 0.356 vs basal out presence of the cycling activity that characterizes the fasting period; p = 0.002 vs. test group). motor pattern. In a recent study using jejunal high-­resolution ma- nometry, we demonstrated that in healthy subjects the postprandial motor pattern induced by a normal meal consists of a combination of 3.6 | Effect on vagal tone continuous segmental activity (i.e., non-­propagated or shortly prop- agated contractions) and intermittent propagated activity, the latter Vagal tone during the basal period was similar in the test and control characterized by single or short bursts of propagated contractions groups, and no changes were detected after gas infusion (RMSSD with higher amplitude than non-­propagated activity.6 The charac- change by −3.7 ± 2.9 ms; p = 0.498 vs. basal) or after sham infusion teristics of the pattern induced by jejunal nutrient infusion in the F I G U R E 4 Effect of colonic filling on postprandial digestive sensations. Colonic filling was associated with a significant increase of digestive sensations, and impaired hedonic response (test group), whereas sham infusion had no effects (control group) ALCALÁ et al. | 7 of 8 present study coincide with those of the postprandial pattern after interpretation of the small bowel manometry. For this reason, it a normal meal. Participants tolerated the nutrient infusion with mild might be recommendable to rule out colonic retention, and if neces- homeostatic sensations, associated to digestive well-­being and pos- sary, clean the colon, before investigating small bowel motility. itive mood, and without discomfort or changes in girth, a response similar to the sensory experience after a comfort meal. These sen- C O N FL I C T O F I N T E R E S T sations also remained steady over the 2-­h nutrient infusion period in No conflicts of interest. the control experiments without colonic gas infusion (sham infusion). Colonic distension was produced by rectal gas infusion. Previous AU T H O R C O N T R I B U T I O N S studies with radiolabeled gas using the same experimental model LA was involved in conduction of studies, data analysis, and manu- showed a uniform distribution of the gas infused along the colon, as script preparation; CM was involved in study design, study manage- well as an effective ileocolic junction preventing gas reflux into the ment, data analysis and manuscript preparation; DML was involved small bowel.3 The colonic gas load in the present study induced ab- in data analysis; FA was involved in study design, data interpretation, dominal sensations, increased girth and reduced digestive well-­being, and manuscript preparation. but did not involve nausea or changes in vagal tone, suggesting that the stimulus did not disturb the physiologic conditions. Indeed, the ORCID volume load (720 ml) was half to that previously tested.5 This colonic Luis G. Alcalá https://orcid.org/0000-0003-3247-1539 stimulus distorted the postprandial motor pattern in the jejunum with Carolina Malagelada https://orcid.org/0000-0001-7097-1492 differential effects on the two motor components: inhibition of non-­ Dan M. Livovsky https://orcid.org/0000-0002-8212-9638 propagated contractile activity and stimulation of propagated fronts. Fernando Azpiroz https://orcid.org/0000-0002-7327-960X The functional implications of the jejunal response cannot be as ascertained, but the propagated fronts resemble the motor pattern REFERENCES that develops in the small bowel proximal to a luminal occlusion. In the 1. Keller J,Bassotti G,Clarke J, et al. Expert consensus document: ad- presence of intestinal obstruction, the proximal small bowel generates vances in the diagnosis and classification of gastric and intestinal motility disorders. 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