Visual parameters define the phase and the load of contractions in isolated guinea pig ileum

Konrad Schulze-Delrieu

Gastroenterologic Research Laboratories, Veterans Affairs Medical Center, Iowa City, Iowa 52242


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

How the movements of the intestinal walls relate to luminal pressures and outflow remains incompletely understood. We triggered the peristaltic reflex in the isolated ileum of the guinea pig and quantified wall movements through computerized measurements of diameter changes. Contractions developed as indentations close to the upstream end of the loop. The indentations deepened and expanded in length. The downstream shoulder of contractions started and stopped to propagate before the upstream shoulder. Shoulders differed in their length and gradient over most of the duration of the contraction, and this gives the contraction an axial asymmetry. Over the course of individual contractions, the length of the indented segment correlated well with the luminal pressure. Contractions in response to large volumes generated long indented segments and high luminal pressures. The onset and the end of pressure waves and of outflow did not necessarily coincide with the onset and end of visual parameters of contractions. These findings indicate that objective visual parameters might be useful to describe and to classify contractions.

peristaltic reflex; intestinal flow; intestinal obstruction


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

DISTENSION OF THE GUINEA pig ileum triggers a contraction, which propagates through the circular muscle layer (19). This stereotypical response, called the peristaltic reflex, has served for many studies on the organization of contractions in the intestine and their control by myenteric neurons (1, 4, 7, 10, 25). Many preparations to study the peristaltic reflex have been described; some recorded luminal pressure, whereas others recorded muscle tension or the outflow of luminal contents (4, 10).

Contractions can also be recognized by the movements of the intestinal wall they produce. The peristaltic reflex produces a characteristic apposition of the ileal walls, which starts at the proximal end of the cut segment and advances in the distal direction (2, 19). We are not aware of detailed descriptions of the visual appearance of these contractions or of systematic studies on the factors that affect the appearance.

In the present study, we used video imaging (16-18) to track wall movements in isolated preparations of guinea pig ileum. We recorded easily identified visual features of contractions as digital data. We then related individual visual parameters to the mechanical and fluid-mechanical parameters of selected contractions.

The specific aims of the study were to 1) identify parameters useful to quantify the visual appearance of contractions, 2) determine how individual visual parameters change over the time course of single contractions, 3) correlate individual visual parameters to luminal pressure and outflow, and 4) determine how visual parameters are affected by the load conditions under which the intestine contracts.


    MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Preparations. The experimental preparation is similar to one we have published before (16-18). Briefly, 15 guinea pigs of either sex, weighing 600-800 g, were euthanized by inhalation of pure CO2. The intestine was exposed through a midline incision. A loop of ileum was taken from 10 to 20 cm proximal to the ileocecal junction, flushed, and cleaned. Cannulas, 3 mm in diameter, were introduced into the proximal and distal ends, and the loop was mounted in a bath containing 500 ml Krebs solution. The composition of Krebs solution was (in mmol/l) 118 NaCl, 4.8 KCl, 2.5 CaCl2, 1.2 MgSO4, 25 NaH2CO3, and 11 glucose. The solution was bubbled with 95% O2-5% CO2 and kept at 37°C. This protocol was approved by the Animal Resource Committee of the Veterans Affairs Medical Center in Iowa City.

The upstream cannula was connected by a three-way stopcock to a syringe, which delivered boluses of specific volume to the lumen (Fig. 1). A three-way stopcock on the downstream cannula was attached to an outflow stub 5 cm high, which emptied into collecting cups. The length of the loop between the upstream and the downstream cannula was adjusted to 10 cm. This length was chosen to allow contractions to move over a maximal distance without having to constantly change the position and angle of the video camera. A force transducer attached to the cup measured the outflow volume (Fig. 1). Residual contents were removed from segments by gentle suction with the syringe, and segments were allowed to recover for a minimum of 5 min between injections. Because injection itself produced flow and movement of segments, the contractions that were regularly triggered by injection were not deemed suitable for image analysis. Rather, the first contraction occurring after the end of the injection was recorded.


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Fig. 1.   Preparation to record contractions in guinea pig ileum. Segments (10 cm) were held in organ bath by cannulas 10 cm apart. They were held 1 cm under the bath surface, with upstream end at left and antimesenteric border pointing up. Pressure sensors were placed into lumen 1 and 9 cm from tip of upstream cannula. Segments were filled from syringe through upstream cannula. Downstream cannula could be opened for outflow through resistance (stub generating 5 cm hydrostatic pressure). Outflow was monitored by calibrated strain gauge weighing the collection cup. Video camera recorded image of anterior wall of ileum. Pressures and outflow were stored as digital data to computer disk and as analog curves on videotapes under picture of moving ileum.

Luminal pressure was recorded by a sensor 1 cm from the downstream end of the loop, consisting of a blunt steel cannula connected by rigid plastic tubing to a Statham Pd 23e pressure transducer. In previous studies, we have found that this distal site develops higher pressures during contractions than more proximal sites (18). The movements of the preparation were monitored by a high-definition color video camera (Sony DXC-960MD).

In the first six experiments, we studied the changes in the configuration of contractions as a function of time and in relationship to luminal pressures and outflow. For this, we used boluses of 1.2 ml and an open outflow. In a second series of experiments, we compared contractions in response to boluses of 0.8 and 1.6 ml. Injections were made into six different preparations, and preparations remained closed to eliminate the effects of changes in luminal volume on configuration. In the last three preparations we recorded the visual parameters of contractions in response to four conditions (0.8 or 1.6 ml, downstream end open or closed).

Transducer signals were processed by a Hewlett-Packard HP 75000 series B VXI Bus and stored as ASCII files to computer disk. The software presents a tracing of the transducer data with a simultaneous numerical display on the computer monitor. A composite of the computer display and video of the preparation were generated by image mixer (Image Labs, model MPS-55II) and a NTSC computer board and recorded on videotape. We reviewed the tapes repeatedly and selected for off-line digital image analysis contractions that met the following criteria: movements of the intestinal wall were related to the effect of the contraction alone and were clearly recorded for the entire contraction. Approximately 30% of all contractions were deemed unsuitable because of movement artifacts from bubbles in the bath, shaking of the baths, or torsion of the ileum to the point that the camera did not faithfully record the contraction.

Definition of visual parameters of contractions. Using diameter measurements at each raster column we defined contractions by the following parameters (Fig. 2A). The length of the contraction is given by the distance between its downstream lead point and its upstream end point; the indented segment is that part of the contraction where the diameter between the mesenteric and antimesenteric walls of the ileum is maximally reduced. In this segment, the two opposing walls run parallel to each other and parallel to the walls of the resting intestine. The indented segment we described by its length and its diameter. The diameter of the receiving segment minus that of the indented segment constitutes the diameter differential the contraction causes. We called shoulders those sections of the contraction that connect the indented segment to noncontracting intestine upstream and downstream. The downstream (leading) shoulder connects the indented segment with the receiving segment; the upstream (trailing) shoulder connects the indented segment with the postcontraction segment. Shoulders are defined by their length (distance from the indented segment to lead or end points of the contraction, respectively) and their gradient. (Gradient is given by the diameter differential divided by length.)



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Fig. 2.   A: visual parameters of intestinal contraction. A 10-cm segment of guinea pig ileum is viewed with upstream end to left and its mesenteric border to bottom. Downstream from contraction is the receiving segment. Here, as in reality, contraction indents mostly the wall of the antimesenteric border. Lead point defines junction between receiving segment and contraction. Downstream shoulder of contraction connects lead point with indenting segment. In indenting segment, mesenteric and antimesenteric walls run parallel to each other, and intestinal diameter remains constant. Upstream shoulder connects indenting segment to end point of contraction. Diameter of receiving segment minus that of indenting segment is diameter differential. Shoulders are defined by length and gradient (gradient is given by diameter differential divided by length). Note that when the 2 shoulders differ in length, the midpoint of indenting segment differs in location from midpoint of contraction, which is halfway between lead point and end point. B: peristaltic contraction in guinea pig ileum. In top frame, at upstream end of preparation, indentation develops along antimesenteric border. In middle frame, indentation deepens; upstream shoulder is short and steep and downstream shoulder long and shallow. Receiving segment downstream from contraction bulges slightly. In bottom frame, length of indenting segment has increased. Shoulders are nearly symmetric at this phase of contraction. Response to injection of 0.80-ml bolus into open ileum 1 s before top frame. Frames are taken 1 s apart.

Contractions move by two processes. One relates to the extension of the indenting segment. The second relates to a downstream movement of the contraction. These two processes do not necessarily occur over the same distance nor do they start and stop at the same time. We therefore recorded propagation of contractions by the downstream movement of 1) the lead of the contraction, 2) its end point, and 3) the midpoint of the indented segment.

Contractions also produce changes in segments adjacent to their site of occurrence. We called receiving segment the part of the preparation that bulges downstream from the contraction. We called postcontraction segment the section of the preparation that the contraction had recently moved through. The length of this section is given by the distance that the end point of the contraction propagated.

Programs to measure visual parameters. We stored contraction sequences on computer disks (JPEG format, sampling rate 4 images/s). To reconstruct the visual parameters of contractions, we used the diameters of all raster columns from the upstream to the downstream end of preparations. We identified the end point of the contraction by the site at which a negative slope is first produced by decreasing diameters. From there we identified the lead point as the site where the slope returns to zero. The edge coordinates are recalled to measure the wall diameters of each image in the sequence. We used an algorithm to determine the ends of the segment and to measure each wall diameter per pixel column along the horizontal length of the segment. We stored all these data in ASCII format on disk. From the digital dates we constructed virtual contractions.

Hardware and programs. Our image analysis system is based on a RasterOps VideoLive Card, a HP 9000 model 735 workstation, and a VCR. We wrote our software in the C programming language using the X Window system and Motif widgets. We extracted the edge of all images in each sequence. We segmented images to a single level threshold. In the resulting binary image the ileum appeared white and the background black. Through morphological outlining we removed all interior pixels of the segment except those that defined its contour. We then used an edge-tracking algorithm to store the contour of the image as a set of Cartesian coordinates to an ASCII file.

Comparisons between experimental conditions were made using Student's t-test. P < 5% was considered statistically significant.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Phases of contractions: relationship of visual parameters to pressure and outflow profiles. Contractions develop close to the upstream end of the loop of ileum and propagate toward its downstream end. Contractions are eccentric around the circumference of the ileum and primarily indent the antimesenteric border (Fig. 2B).

We defined three sequential phases to characterize the waxing and waning of contractions: 1) the developing, 2) the expanding, and 3) the vanishing contraction (Fig. 3). During the developing phase, the antimesenteric wall moves toward the mesenteric wall; this phase ends when the diameter is maximally reduced and the indented segment is established (Fig. 3B). During the expanding phase of the contraction, the contraction moves along the length of the ileum and the length of the indented segment increases (Fig. 3C). The diameter of the indented segment remains the same during the expanding phase and widens when the contraction vanishes (Fig. 3B). The length of the contraction may still increase to drop off abruptly once the diameter returns to baseline (Fig. 3C). Pressures and outflow cease well before the visual end of the contraction.


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Fig. 3.   Visual parameters during phases of single contraction. A: profile of pressure and outflow. Outflow surges during pressure wave at between 7 and 12 s and ceases as pressure returns to baseline. B: diameter and pressure. Diameter of indenting segment mirrors that of pressure wave. Three phases of contractions can be distinguished: in initial phase of the developing contraction, diameter narrows and pressure rises. During the second phase of the expanding contraction, pressure peaks and diameter remains at nadir. The third phase of the vanishing contraction is characterized by pressure decline and an increase of diameter toward but not up to baseline. C: length of contraction in relation to pressure. Length increases more slowly and steadily than pressure and peaks after pressure. Length maintains a plateau, before it drops off sharply more than 2 s after pressure has returned to baseline. D: diameter of indenting segment in relation to outflow. Outflow occurs during reduction of diameter of indenting segment. E: correlation of length of contraction with outflow profile. Length of contraction rises roughly in parallel with outflow. F: gradients of shoulders superimposed on pressure profile. Upstream shoulder develops a gradient which peaks and disappears in parallel with pressure profile. Gradient of downstream shoulder is steep before and after pressure wave. G: correlation of shoulder gradients with outflow. Peak of downstream gradient coincides with onset of outflow.

The gradient of the upstream shoulder changes virtually in parallel with the luminal pressure (Fig. 3F). The gradient of the downstream shoulder peaks before the onset and again after the end of the pressure and outflow (Fig. 3G). Differences in the gradients of the two shoulders create an axial asymmetry of the contraction (Figs. 2B and 3G).

Visual parameters of contractions as function of time or location. The appearance of contractions changes with time and with their location along the segment of ileum. Figure 4 shows how a contraction forms a short indentation close to the upstream end of the segment during the upstroke of the pressure wave and a long indentation close to the downstream end of the segment during the pressure peak.


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Fig. 4.   Appearance of contractions and of pressure curves in response to different bolus volumes. A: contraction response to injection of 0.8-ml bolus. Injection terminated at 45 s. Pressure starts rising at 46.2 s and returns to baseline at 52.2 s. During this period, an indentation forms on antimesenteric border, widens, and moves downstream. Broken line connects lead point of contraction and solid line end point of contraction, which our analytic program identified. Between 47.2 and 49.4 s lead point advances faster than end point as contraction simultaneously widens and propagates. As contraction approaches downstream end of the preparation, bolus escapes and produces a bulge in postcontraction segment and second pressure peak. B: contraction response to 1.6-ml bolus. Segment over which contraction indents preparation is longer and moves a shorter distance downstream than with 0.8-ml bolus. Pressures in distal sensor exceed 20 mmHg. Widening of receiving segment is more pronounced here than with 0.8-ml bolus.

Virtual contractions are renditions of select visual parameters of the contraction at specific points in time and facilitate the recognition of movement patterns. Figure 5 shows how the length of the indented segment first increases and then decreases over the course of the contraction and how the gradient of each shoulder changes independently from the other. Table 1 gives numerical data on specific parameters at specific points in time. This also shows that the midpoint of the indented segment propagates steadily up to the end of the contraction, whereas the lead point propagates swiftly at first and then slows and stops.


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Fig. 5.   Virtual configurations of contractions as function of load conditions. Contractions were reconstructed from automated analysis of visual parameters. Their visual patterns are charted at specific points in time and at site of 10-cm segment at which they were then located. Each composite line is a proportional rendition of the length of the indenting segment and of the gradients and length of the shoulders. A: injection of 0.8-ml bolus into open preparation. Occluding segment moves at a fairly steady rate from about 4 to 9.5 cm; its length increases steadily up to 2 s and then steadily decreases. B: injection of 1.6-ml bolus into open preparation. This generates contraction of considerable length. Much of the length is made up of the shoulders. Shallow gradient of upstream shoulder indicates that postcontraction segment remains fairly collapsed. C: response to 0.8-ml bolus into closed segment. In first 2.0 s, the lead point advances as indenting segment lengthens. Between 2.0 and 2.5 s contraction suddenly shifts into distal half of preparation and deeply indents lumen. This presumably reflects distension of both receiving and postcontraction segment by fluid. Length and gradient of downstream shoulder increase, indicating a bulging receiving segment. D: response to 1.6-ml bolus into closed segment. Contraction moves over a shorter distance than when preparation is open.


                              
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Table 1.   Visual parameters of contractions as functions of time and load

Contraction in response to varying loads. Increases in bolus volume lead to changes in the visual parameters of contractions, which parallel changes in luminal pressures. An example characteristic of the responses to injecting 0.8- and 1.6-ml boluses into the same closed preparations is shown in Fig. 4. Pressures are higher, the contracting segment is longer, and the distance the contraction propagates is less with the larger bolus. The increasing length of the contraction reflects an increase in the lengths of the downstream shoulder and of the indented segment (Fig. 5, Table 1).

Contractions in response to small bolus volumes against low resistance generate shallow, short, and symmetric indentations that move quickly along the preparation (Fig. 5A). Contractions in response to large bolus volumes are characterized by long and deep indentations with a long leading shoulder (Fig. 5B). In a closed preparation, propagation appears slow at first until it gets a sudden boost as the bolus escapes retrograde (Fig. 5C). Alternatively, in a closed segment, there may be massive bulging of the receiving segment (Fig. 5D). Also, in closed segments, the length of the indenting segment increases to a maximum at between 1.5 and 2.0 s and declines thereafter (see Table 1). This is unlike in open preparations where emptying mediated by the contraction may produce a lasting reduction of the diameter (Fig. 3, B and C, for example).


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

In the present study, we describe intestinal contractions by visual criteria, which can be constantly monitored and analyzed as digital data. We then studied how visual parameters change over the course of individual contractions in the isolated guinea pig ileum and how they relate to simultaneous recordings of luminal pressure and outflow. We tested how the parameters are affected by the bolus volume injected into the intestinal loop and by whether the end of the loop is open or closed. Our data suggest that objective visual parameters can be used to characterize the phases of individual contractions and to compare different contractions.

The configuration of contractions described in our analysis may have implications for the biomechanical properties of the intestinal wall (9), the neurosensory mechanisms controlling the contraction responses (1, 4, 7, 10), and the mechanics of luminal flow (2, 11-14, 24). We found that contractions indent primarily the antimesenteric wall of the guinea pig ileum. Several recent studies on the neuronal controls of the peristaltic reflex used videotapes and experimental conditions similar to ours (20-23). However, Tsuji et al. (20) restricted visual analysis of contractions to their propagation in full-thickness intestine compared with that in intestinal tubes devoid of mucosa and submucosa. Waterman and co-workers (21, 23) restricted visual analysis to diameters at select points of the segment at specific points in time. Neither group commented on the eccentric nature of the indentation caused by contractions. That contractions of the small bowel often take an eccentric configuration has been shown before, including in the in situ duodenum of the human and the cat (3, 6, 8, 15-18, 23, 25). One possible explanation for the circumferential asymmetry of contractions is the eccentric thickness of ileal muscle coat recently reported by Cue et al. (5).

We also found that contractions were asymmetric along the axis of the ileum. The axial asymmetry reflected the different rates at which the indenting segment expanded and at which the contraction propagated along the intestine. Thus the lead point moved downstream before the end point; once the lead point stopped the end point would catch up. Circumferential and axial asymmetry are likely to have implications for luminal flow. The analytic work that has been done on the fluid-mechanical implications of intestinal contractions made the assumption that indentations of the intestinal wall are concentric and symmetric (9, 11-14, 24).

Our observations indicate that the configuration of contractions changes with volume load and outflow resistance. It is likely that factors such as the specific gravity, compressibility, and viscosity have similar or additional effects on the configuration of contractions. It remains possible that different experimental conditions would eliminate the axial or circumferential asymmetry observed here. For the sake of imaging we prevented segments from shortening. Longitudinal contraction is an important part of the peristaltic response (1, 4, 7, 19, 25), and shortening might well change the configuration of the contraction.

The changes that contractions imparted on the intestinal configuration went through three characteristic phases: 1) they developed as shallow indentations that deepened until the lumen was maximally reduced, 2) they expanded as the diameter reduction included an increasingly long segment of the intestine, and 3) they vanished by the incremental increase of the luminal diameter toward but not necessarily fully back to baseline. Narrowing of the lumen resulted in outflow and luminal pressure.

The timing between the visual and the mechanical changes was complex. Visual parameters identified contractions over longer time periods than did pressure or outflow parameters. For instance, indentations typically preceded the rise of luminal pressure, and some contractions aborted during this initial phase. Thus the beginning of contractile activity appears to be reflected more accurately in the indentation than in the luminal pressure, which is dampened at first by outflow or downstream accommodation.

Even greater divergence was observed for the cessation of contractile activity. Pressure dropped back to baseline apparently before the end of contractile activity, whereas visual changes persisted until after their end. Pressures were again affected by accommodation and outflow. The visual end of contractions depends largely on refilling of the postcontraction segment. As it advances, the contraction leaves the postcontraction segment behind it empty and collapsed. If the contraction clears the lumen permanently of contents, the indenting and postcontraction segment might increase in length and merge until they involve the entire length of the intestinal preparation. Thus the postcontraction segment assumes the resting diameter of the empty intestine. The situation is different if the segment continues to contain or to receive luminal contents. For instance, if contractions are prevented from emptying contents from the distal end of the segment, redistribution of volume occurs. In that situation, refilling of the postcontraction segment actually reduces the length of the indenting segment long before the end of the contraction.

Pressure changes parallel changes in the length of the indented segment. Contractions that produce high luminal pressures also produce long indented segments. This finding reflects the expected close association between lumen occlusion and the mechanical effects of contractions. It implies that a primary mechanism by which the intestine copes with increased loads is to recruit additional lengths of the intestine to contract. We have previously demonstrated contractions of increasing length and force with retrograde perfusion of the duodenum (16). To what extent correlations between force of contractions and length of indenting segment apply in other gut segments and across a variety of preload and afterload conditions remains to be studied.

The length and the gradients of the shoulders of the contraction were also influenced by the conditions in the receiving and the postcontraction segment. If a great amount of fluid accumulated in either segment, the slopes connecting the indented segment to them could become quite long or steep.

Isolated loops of guinea pig ileum have long been used to study various aspects of intestinal contractions (1, 4, 7, 10, 16-23, 25). One limitation of these preparations is their comparatively short length. Contractions are likely to differ if they and the luminal contents they drive can advance unimpeded over long distances or if they come to a rapid end at a mechanical barrier (24). As a compromise, we used here segments as long or longer than used in most studies of the peristaltic reflex. This ensured that our data can be compared with that literature (1, 4, 7, 10, 16-23, 25). In humans and in intact animals, non-lumen-occluding contractions are common and may represent the majority of contractions after meals (6, 8, 15). To what extent our observations can be extended to contractions that do not produce occlusion of the lumen as did apparently most contractions in our preparation remains to be studied. We do not suggest, in this regard, that the term indented segment be reserved only for contractions that occlude the lumen.

We conclude that parameters derived from computerized measurements of intestinal diameters can be used to define contractions in objective visual terms. Visual parameters can be used to describe the temporal phases of contractions and their geographic progression along the intestine or to compare contractions that occur under different conditions. Of select visual parameters, the length of the indented segment shows particular promise as a predictor of the mechanical effectiveness of contractions.


    ACKNOWLEDGEMENTS

John Raab, Dept. of Surgery, Univ. of Iowa, wrote the software and did data processing. Bob Hermann performed experiments and data collection. Drs. Siroos Shirazi, Dept. of Surgery, and Bruce P. Brown, Dept. of Radiology, provided critical support.


    FOOTNOTES

This work was supported by a Merit Review Grant from the Veterans Affairs Medical Center.

Address for reprint requests and other correspondence: K. S. Schulze, Digestive Disease Center, 4551 JCP, Univ. of Iowa, Iowa City, IA 52242 (E-mail: konrad-schulze{at}mail.int-med.uiowa.edu).

Received 10 July 1997; accepted in final form 1 March 1999.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

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Am J Physiol Gastroint Liver Physiol 276(6):G1417-G1424