GASTROENTEROLOGY
1990;99:1009-1015
Sensory and Motor Responses to Rectal Distention Vary According to Rate and Pattern of Balloon Inflation WE1 MING SUN, NICHOLAS W. READ, ALISON JO-ANNE DALY, S. KEVIN CHEAH, and DAVID Subdepartment of Gastrointestinal Sheffield, England
PRIOR, GRUNDY
Physiology and Nutrition, Royal Hallamshire
Anorectal motor activity and rectal sensation were recorded in 12 normal male subjects during ramp distention of the rectum with water and air at randomized rates of l&20, 50, and 100 mL/min and during intermittent rapid distention with air. There were no significant differences between the results of ramp inflation with water or with air, and the repeated infusion of the same medium yielded reproducible results. Ramp distention induced sigmoid pressure-volume profiles. Different sensations occurred at specific points on the pressure-volume curve and were maintained until succeeded by the next sensation. Initial perception of the distention occurred during the initial steep pressure increase, the sensation of wind occurred during the plateau phase, and the desire to defecate occurred at the onset of the final rapid ascent. Rectal sensations were induced at lower volumes at low infusion rates when the slope of the pressure-volume relationship was shallower than at high infusion rates. This suggests that the receptor triggering rectal sensation is not a simple volume or pressure receptor, but is more likely to be a slowly adapting mechanoreceptor lying parallel to the circular muscle of the rectal wall. During rapid intermittent distention, the rectal volumes required to elicit rectal sensations were lower than during ramp distention, although the pressure-volume curve was steeper. Moreover, sensations often only lasted a short period of time but recurred on deflation. These data suggest activation of an additional population of rapidly adapting or high threshold mechanoreceptors. Anal relaxation was always evoked by intermittent rectal distention and was almost always associated with a rectal sensation and an increase in external anal sphincter activity. In contrast, anal relaxation could be absent or delayed during ramp inflation, especially at lower infusion rates, suggesting that internal sphincter can
Hospital,
maintain continence for a long period of time while the rectum is slowly filling. Rectal sensation and concomitant external anal sphincter activity was not associated with anal relaxation during ramp inflation; most subjects felt the sensation long after the pressure reached its lowest level. However, under all circumstances the onset of rectal sensation was associated with an increase of external anal sphincter electrical activity. In conclusion, the rectal sensory and anorectal motor responses to distention depend on the rate and pattern of distention, which may activate a different population of receptors. Results from different laboratories cannot be compared directly unless the pattern and rate of distention are the same.
alloon distention of the rectum is an accepted simple method of measuring rectal compliance and evoking rectal sensation and reflex activity of the anal sphincter (1,2). Abnormal responses to balloon distention have been reported in patients with incontinence (3,4), diabetes mellitus (5), constipation (6,7), megacolon (8,9), multiple sclerosis (lo), fecal incontinence (in elderly patients) (ll), colitis (12,13), solitary ulcer syndrome (14), and irritable bowel syndrome (151, but results from different centers show a wide degree of variation which is generally thought to be related to differences in methodology. Different groups use balloons that are of differing shapes and sizes, inflate with different materials [air or water], use differing types of distention (ramp inflation at a continuous constant rate of infusion, stepwise increments,
B
Abbreviations used in this paper: EM, external anal sphincter; IAS, internal anal sphincter; MI, motility index. 0 1990 by the American Gastroenterological Association 0016-5035/90/s3.00
October 1990
intermittent distention with different volumes) and differing rates of inflation, and record responses in different ways. In a recent workshop (16), it was recommended that ramp inflation of the rectum would provide the most useful method to elicit sensory and motor responses because the rate of distention can be easily controlled. Does ramp distention test the same aspects of anorectal function as intermittent distention, and is the rate of rectal distention an important variable? No systematic study has been performed to answer these questions. It is commonly assumed that rectal distention elicits sensory and motor responses by triggering sensory receptors in the rectum or pelvic floor muscles. The precise nature of these receptors is not known. The rectum receives a dual afferent supply from the pelvic and lumbar splanchnic nerves. Electrophysiological studies in experimental animals have identified different populations of rectal mechanoreceptors that respond to distention and/or contraction and show a range of thresholds, firing rates, and rates of adaptation (17-19). Some respond to rapid changes and accommodate quickly to the new steady state and others respond to a more gradual change and continue to fire for long periods as the stimulus is maintained (18,191. It seems likely that both may coexist in the rectum and may show differential responses according to the rate of distention. The purpose of this study was to investigate how anorectal responses to rectal distention varied according to the pattern and rate of distention and also to the nature of the distending medium. The data provide some interesting insights into the nature of the rectal receptor mechanisms. Materials and Methods Subjects Twelve normal male volunteers (aged 20-25 years: median age, 22 years] who had no history of bowel disease were studied. A written consent form was obtained for the test to be performed. The protocol was approved by the Ethical Subcommittee of the Sheffield Health Authority in June 1988. Studies were performed at the same time of the day on three occasions separated by at least 1 week. No bowel preparation was used although subjects were encouraged to empty the rectum before the test if they felt the need to do so, and a digital examination of the rectum was performed immediately before the test to ensure that the rectum was empty.
Methods The subjects were lying in the left lateral position with the hips flexed to a go-degree angle, and a manometric probe consisting of a polyvinyl 7-lumen tube with an
VARIABLE
RESPONSES
TO RECTAL DISTENTION
1009
external diameter of 4 mm was inserted into the rectum. When correctly positioned, manometric side holes were situated in the anal canal at approximately 0.5, 1.0, and 2.0 cm from the anal verge and in the rectum at 4.5 and 15 cm. The side holes were perfused with water at a rate of 0.4 mL/min by a low-compliance pressurized perfusion system (Mui, PIP 2, Mississauga, Ontario, Canada], and pressures were measured by pressure transducers (Statham 23ID, Oxnard, CA) that were situated in each perfusion line and connected by means of amplifiers to a multichannel chart recorder (Hewlett Packard 7758A, Waltham, MA]. A highly compliant, thin-walled balloon constructed from a 6-cm cylinder (diameter = 5 cm] of unstretched condom (Durex Dry; LRC Products Ltd., London, England] was tied to the probe 5-11 cm from the anal verge. The pressure within the balloon was measured by a water-filled, nonperfused catheter connected to a transducer. The electrical activity of the sphincter was recorded using bipolar electrodes consisting of two trimel-coated wires (diameter, 0.025 mm) with their ends bared, hooked, and offset to avoid electrical contact (20.21). Two pairs of electrodes were inserted with the aid of a hypodermic needle, one into the superficial external anal sphincter (EAS) and the other into the internal anal sphincter (IAS). The EAS electrode was attached to an amplifier (differential type 2lCOl; URO-DISA, Copenhagen, Denmark), which was connected by means of an integrator (AC to RMS convertor; Analog Devices AD536,170 ms time constant, East Molesey, England) to the chart recorder. The IAS electrode was connected to the chart recorder by means of an amplifier (filter, 0.5-10 Hz). The activity of the IAS was represented on the raw electromyograph record as a regular oscillation which occured at a frequency of between 10 and 24 oscillations per minute and increased in amplitude as the activity of the muscle increased and vice versa. The integrated activity of the EAS was represented as an elevation above the base line.
Protocol Anorectal pressures were recorded under resting conditions for 20 minutes until they reached a steady state. Rectal distention was then performed. Each subject had 11 rectal distentions performed at three sessions. The balloon was inflated with air at a constant rate of 10, 20, 50, and 100 mL/min by means of a nitrogen gas cylinder equipped with a regulator or was inflated with water at the same rates by means of a peristaltic pump (Minipuls 3, Gilson 312, Villiers Le Bel, France]. The order of the ramp inflations was randomized. Both water and air were infused at room temperature. Inflation with water at the rate of 10 and 20 mL/min was performed on two separate occasions to test the reproducibility of the results. In each case, distention would continue until the subject complained of discomfort, and a gap of at least 20 minutes was allowed between inflations. Intermittent rapid distention of the rectum was performed by inflating the balloon at a rate of about 40 mL/s with volumes of 10, 20, 40, 60, and 100 mL of air by means of a handheld syringe. Each inflation was maintained .for 1 minute, then the balloon was deflated and a gap of at least 1 minute was allowed before the next inflation.
1010 SUN ET AL.
GASTROENTEROLOGY Vol. 99,No. 4
During rectal distention, subjects were instructed to report their initial perception, to report the onset of a feeling of gas in the rectum [wind) and the desire to defecate, and to indicate the onset and the duration of the sensation on the chart using a remote event marker. The lowest distending volumes at which the balloon was perceived and the lowest volumes required to induce a feeling of wind, a sensation of desire to defecate, and a sensation of discomfort or pain were recorded. The pressure-volume characteristics of the balloon at different rates of infusion of air and water were tested ex vivo before the start of each test. Those values were subtracted from the graph relating rectal balloon pressure and volume to yield values for rectal pressure at each distending volume. From these profiles, the slope of the rectal pressure and volume relationship was measured, and values for rectal compliance (dV/dP, mL/cm H,O) from 0 to 100 mL were also calculated. The motility index [MI) during balloon distention was expressed as the area under the manometry record from the rectal side-opening port.
Statistical
mL/min but was near the top at 100 mL/min (Figure 1). The perception of the sensation of wind occurred during the plateau phase and lasted while the pressure remained steady. The change in slope to the final rapid ascent was associated with the perception of a desire to defecate [Figure 1) and pain and discomfort was perceived during this final rapid ascent. The pressures for a given increment of volume were significantly lower (P < 0.05) at lower infusion rates (Figure 2). Thus the rectum was more compliant at a lower infusion rate than at a higher infusion rate [Figure 2). However, each sensation was perceived at lower volumes and at lower pressures when the infusion rate was slower (Tables 1 and 2) (Figure 1). Each different sensation was continuous until it was superceded by a new sensation. The lowest volumes required to cause rectal sensation, the sensation of wind, the desire to defecate, and discomfort were similar during either air or water infusion [Table 1). Moreover, the rectal pressures recorded at each particular rectal sensation [Table 2), the initial slope of the pressure increase, and the rectal compliance at each infusion rate did not show any significant differences between distention with water and distention with air (Figure 2). Repeated rectal distention with water at 10 and 20 mL/min showed similar results for rectal compliance (r = 0.62) and volumes and pressure for which initial perception (r = 0.91), desire to defecate (r = 0.931, and discomfort (r = 0.79) were perceived [Figure 3). The pressurevolume characteristics of the balloon were identical at the four infusion rates and irrespective of whether air or water was being infused (r > 0.99). Inflation of 50 mL of either air or water increased pressure by approximately 22 cm H,O; increasing volumes up to 300 mL caused no further pressure increments. Recordings from rectal side-opening ports. The pressures recorded in the rectal side holes increased as the distending volume increased. This pressure
Analysis
The statistical significance of the differences was determined by the F test. The correlation between the different treatments was examined by Pearson’s r test. The x2 test was used to analyze the percentage of subjects who showed certain phenomena at different rates of inflation.
Results Ramp
Inflation
Rectal pressure-volume relationship. The pressure-volume relationship during ramp inflations had a characteristic triphasic curve irrespective of the rate of inflation. This consisted of an initial steep increase followed by a plateau and a final rapid ascent [Figure 1). Different rectal sensations were perceived at different points on the curves. Initial perception of the distention occurred at the middle part of the steep aspect of the pressure increase at rates of 10.20, and 50
0
/
A
1.’ ,’ ,.,’
,I.’
5b Distension
volume
(ml)
100
150
200
Figure 1. Pressure-volume characteristics (A)during rectal ramp inflation with water at the rates of 10 (-+ 20 (-), 50 (-), and loo (. . . . .) mL/min and, (B) at the intermittent distention (- . . -1 with air. Data are the mean values of each distention. Arrows indicate where perception of the ballaon ( I), feeling of wind ( f ), and desire to defecate ( j ) I were felt.
VARIABLE RESPONSES TO RECTAL DISTENTION
October 1990
ab
a
1 a
ab
abc
defecate and discomfort were felt. These rapid increases were associated with repetitive contractions (Figure 4). The amplitude of rectal contractions was greater at higher infusion rates. However, when the motility indices were normalized to the same increments of volume, there were no significant differences (P > 0.05) between the different rates of infusion (Table 2). Motility indices during infusion of air and water at the same rates were also very similar. Anal responses. Fifty-eight percent of subjects showed no anal relaxation at all when the inflation rate was 10 mL/min, and 17% showed no relaxation at an inflation rate of 20 mL/min (P < 0.05 compared with 10 mL/min). All subjects showed anal relaxation at the inflation rates of 50 and 100 mL/min (P < 0.001 compared with 10 mL/min). Thirty-three percent of subjects showed anal relaxation within 3 seconds of the onset of the inflation at the inflation rates of 50 and 100 mL/min, 25% at 20 mL/min, and 17% at 10 mL/min. When relaxation occurred, the average delay in onset of relaxation was 68 + 2 seconds at 10 mL/min (P < 0.05 compared with 20, 50, and 100 mL/min), 35 c 10 seconds at 20 mL/min (P < 0.02 compared with 50 and 100 mL/min), 14 f 4 seconds at 50 mL/min (P < 0.05 compared with 100 mL/min), and 7 f 2 seconds at 100 mL/min. Anal relaxation was always associated with diminution of the amplitude of the IAS slow wave. At an infusion rate of 10 mL/min, five subjects perceived the balloon before the anal relaxation occurred, three at 20 mL/min and two at 50 mL/min. The rest of the subjects did not feel the sensation until long after the anal pressures reached the lowest steady state. None of the sensations occurred as the anus relaxed. The electrical activity of the EAS remained at basal levels as long as distention had not been perceived. Perception of the balloon was associated with an increase in the electrical activity of the EAS, and the
abed
1 a bc
I abed
1
I
100 intermittent
Perfusion
rate
1011
( mllmin)
Figure 2. Relationships between different perfusion rates and (A) theinitial slope of the rectal pressure increase and (B) the rectal compliance at the rectal volume of 100 mL The results obtained from water @) and air ( ?) ? inflation were compared. “Signi5cantly different than 10 mL/min, bsigni8cantly different than 20 mL/min, %ignificantly different than 50 mL/min, and dsigni5cantly different than 100 mL/min (P < 0.05). For intermittent rapid dietenHan, the steady-state pressure was plotted.
was greater in the high rectum (15 cm) than in the lower rectum (4.5 cm] [Figure 4). The pressure increase was gradual at first but increased rapidly just before (t5 seconds] or at the same time as the desire to
increase
Table 1. Comparison of the Lowest Rectal Volumes Required to Elicit Rectal Sensations Between Ramp Distention at Different Rates and Rapid Intermittent
Distention Inflation rate (mL/min] 20
10
Rectal volume (mL) Perception Wind Desire to defecate Discomfort
Water
Air
15 f 4 40 f 3 118 + 15 160 * 14
15 * 4 42 + 4 120 * 14 163 * 17
NOTE. Data are expressed “Significantly different from bSignificantly different from “Significantly different from dSignificantly different from
as mean * SEM. 10 mL/min. 20 mL/min. 50 mL/min. 100 mL/min.
Water 20 f 50 f 130 f 178 f
6 10 12 20
50 Air 20 + 5" 51 * 9" 128 f 10" 178 + 20’
Water 24 + 64 f 160 f 199 *
6 10 19 24
100 Air 22 *4"b 62 +9* 158 * 8& 210 zt 24*
Water 40 ilO 80 f 11 175 + 10 216 i 20
Air
Intermittent Air
43 * 1o*b" 12 * l"bCd 81 + gab= 27 + 4*cd 167 2 7&" 75 f 10*Cd 230 * 21&” 110 * lo&cd
GASTROENTEROLOGY
1012 SUN ET AL.
Table 2. Comparison of the Lowest Rectal Pressures Associated With Rectal Sensations Between
Ramp Distention
at Different
Rates and Rapid
Intermittent
Vol. 99, No. 4
and the Rectal Motility Indices
Distention
Inflation rate (mL/min) IO
Rectal pressure (cm H,O) Sensation Wind Desire to defecate Discomfort Motility index (mm”/min) NOTE. Data “Significantly bSignificantly “Significantly dSignificantly
20
100
50
Water
Air
Water
Air
Water
7*1 IO + 3 13 * 2 18 f 2 61 + 20
7&l 11 f 4 14 k 2 18 zt2 62 f 20
IO + 2 15 + 2 18 i:2 22 + 3 71 k 25
11 km2" 14 f 3O 19 f 2O 22 + 4" 75 * 25
13 + 2 17 * 3 22 f 3 30 + 4 70 f 25
Air
13 *1* 16 t 3* 22 + 3"b 33 *4* 80 k 23
Water
Air
18 + 3 22 f 2 29 * 4 36 f 5 100 i 30
1922h 21 + 1*c 28 + 4&' 38 k 70bc 98 f 30
Intermittent Air 13 f l*d 21 + 3"bc 30 f 3"bc 37 k 5"h"
are expressed as mean * SEM. different from IOmL/min. different from 20 mL/min. different from 50 mL/min. different from 100 mL/min.
increase was maintained or enhanced as the infusion volume increased (Figure 4). The onset of each new sensation was associated with a burst of EAS electrical activity (Figure 4). Intermittent
Distention
Rectal responses and sensation. Intermittent balloon inflation with increasing volumes of air was associated with an initial increase in pressure in the rectal balloon as the air was introduced. This was often followed by a transient secondary increase in pressure. The pressure then gradually subsided to a steady state. Rectal pressure increased in amplitude and duration as the distending volume increased. The
. .
Discomfort
DD
Perception rz0.96
pressure changes for given pressure increments were significantly greater during intermittent distention (P < 0.05) than during ramp inflations (Figure l), and rectal compliance was consequently much lower (P < 0.05) during intermittent distention (Figure 1). The pressures recorded by the rectal side holes showed components similar to those in the balloon channel. Repetitive rectal contractions were seen in the rectal channels when the desire to defecate was experienced. The amplitude of contractions was larger in the upper rectal channel than in the lower rectal channel. The relationship between steady-state pressure and volume during intermittent distention also consisted of three components: an initial rapid increase, a slower increase, and a final rapid ascent. Rectal
rc0.93
200
.
.
. .
r zO.82
300
.’. . ..
0
50 Rectal
volume
r-=0.96
50 1
50
. *. ‘.
. a.
.
.
. .
50
0
20 Rectal
pressure (2nd
*.- . .
300
(ml)
(2nd value)
rz0.91
.
(cm H20)
value)
.; * . .L. %. r=0.79
0
50
Figure 3. Diagram to illustrate (A) the reproducibility of the repeated measurements of rectal volume required to elicit rectal sensation end (B) the rectal pressures required to elicit different rectal sensation at the inflation rate of 20 mL/min.
October
VARIABLE
1990
Channel
c”lzO 320
1
l----
0
60 6 0
-
I
I ntogated EMG
k
t felt
wind
tt
dd discor%
RESPONSES TO RECTAL DISTENTION
1013
decline in anal pressure that was usually observed in all anal channels and was associated with the suppression of IAS electrical oscillations. All subjects showed anal relaxation at a distending volume of 10 mL (compared with 5 of 12 during 10 mL/min ramp inflation: P -C0.001). As the rectal volume increased, the electrical activity of the EAS increased in amplitude and duration, while the anal pressure decreased in amplitude and increased in duration. The EAS activity was tightly linked to perception during intermittent rectal distention. Two subjects, who did not feel the distention with 10 mL of air, did not show any electrical activity of the EAS. Similarly, subjects did not perceive the sensation if the distention did not elicit rectal contraction. The duration of rectal contraction, rectal sensation, and EAS activity were closely related (r > 0.8). Upon deflation of the balloon, the anal pressure often increased to values that were higher than the preinflation pressures. The rebound increases in pressure lasted at least 1 minute when rectal volumes exceeded 60 mL and were always associated with increases in the amplitude of the IAS slow wave.
.)
Figure 4.
Recordings of anorectal pressures at ports
situated at 0.5,
and 15 cm from the anal verge and in the rectal balloon (5-11 cm from the anal margin) [channels l-6)and the integrated electrical activity of EAS(channel7] during ramp inflation with air at the rate of 50 mL/min. Note that (a) the rectal pressures increased during the rectal inflation and the pressures recorded at higher rectal channels are higher than at lower ones, (b) the rectal pressures increased when desire to defecate (da) and discomfort were felt, and (c] an increase in electrical activity of the EAS was associated with the onset of each specific rectal sensation. 1.0,2.0,4.5,
sensation was perceived during the initial rapid increase, a sensation of wind was felt at the beginning of the slow increase (presumably corresponding to the plateau during ramp inflation), and the desire to defecate was experienced when the pressure started to climb steeply again. Despite the lower compliance, the rectal distending volumes required to elicit rectal sensations were significantly lower (P < 0.001) during intermittent distention (Table 1). All subjects felt a rectal sensation during inflation at 20 mL, and all except two subjects perceived the balloon at 10 mL. At low volumes, a transient sensation was experienced as the balloon was inflated, and a similar transient sensation was perceived as the balloon was deflated. The sensation became more prolonged as the distention volume increased. Anal responses. Intermittent distention of the rectal balloon caused a transient increase in anal pressure, seen most clearly in the outermost anal channels and associated with an increase in the electrical activity of the EAS. This was followed by a
Discussion The results of this study show that the sensory and motor responses of the rectal distention are affected by the rate and pattern of distention but not by the change of medium (water or air). Repetitive distention at the same rate shows a high degree of reproducibility, as previously reported by Varma and Smith (22). Ramp inflation generates a sigmoid pressure profile. The early rapid increase presumably reflects the elastic properties of the tonically contracted bowel and ends in a plateau phase, presumably when the distending stimulus induces receptive relaxation. The final increase occurs at the limits of relaxation and represents the elastic properties of the relaxed bowel. Irrespective of the rate of distention, the sensory experiences of rectal distention, which range from sensation of wind to desire to defecate to discomfort, are closely associated with the rectal pressure profiles observed during distention. Initial sensation was first experienced during the initial rapid increase in pressure. A feeling of “wind” occurred near the beginning of the plateau when the rectum was relaxing to accommodate the increasing volume, while a desire to defecate occurred when the rectum reached its limit of accommodation and pressure began to increase steeply again. Rectal sensation and anorectal motor responses varied according to the rate of ramp inflation. Increasing the rate of inflation produced graded increases in pressure at each volume, suggesting that the time-
1014
SUN ET AL.
dependent relaxation of rectal smooth muscle is overcome at higher flow rates. Moreover, rectal sensations were perceived at lower volumes when the infusion rate was slower and pressures were lower. These results are incompatible with a simple volume or pressure receptor; instead they suggest the activation of a slowly adapting mechanoreceptor within or on the rectal wall. Such a receptor would be subjected to a greater degree of stimulation when the rectum relaxes; relaxation occurs earlier and at lower volumes when infusion rate is slowest. This arrangement is facilitated by the tubular nature of the rectum. When lateral expansion of the balloon is limited by tonic contraction of rectal smooth muscle, the balloon can still extend in a longitudinal direction. In this way, rectal receptors are protected from circumferential stretch at high rates of distention and a greater rectal volume can be tolerated. The facility for longitudinal extension of the balloon would also explain why distention with a compressible gas yields results that are virtually identical to those obtained when the rectum is distended with a less compressible liquid. Rectal sensations were perceived at much lower volumes during intermittent rapid distention of the rectum than during ramp inflation. However, at low volumes the sensations did not last for the duration of the distention. One possible interpretation is that rapid distention stimulates an additional population of rapidly adapting mechanoreceptors. If this is correct, then the perception of a transient sensation when the balloon is both inflated and deflated is compatible with the behavior of mucosal receptors stimulated by the rapidly expanding or contracting balloon (23). An alternative interpretation is that intermittent distention activates a high threshold receptor, which only fires at the initial peak in rectal pressure that occurs as the balloon is inflated. In this regard, we have previously described a close correlation between the duration of transient peak in rectal pressure induced by rapid intermittent distention and the duration of sensation (2). It is perhaps simplistic to presume that rectal perception is induced by activation of a single population of mechanoreceptors. It is likely that the final conscious perceptions of rectal distention arise from a combination of sensory inputs with reflex responses to the distention modulating the sensory experience. Sensation may be modulated, for example, by the changes in rectal compliance observed at different rates of distention, stimulation of mucosal receptors, and activation of receptors in the high rectum or sigmoid colon caused by longitudinal extension of the balloon. In this study, the urge to defecate was associated with increased contractile activity in the proximal pressure port. However, there was no temporal relationship
GASTROENTEROLOGY
Vol. 99, No. 4
between rectal sensation and the onset of anal relaxation. There are also important differences between the anal responses to intermittent and ramp distention of the rectum, and these may also relate to activation of different populations of receptors. Intermittent distention induced a prompt relaxation of the IAS and a contraction of the EAS that was closely associated with sensation and always occurred at volumes that were equal to or lower than those that elicited anal relaxation. Thus the threat to continence produced by rapid entry of fecal material into the rectum, the high rectal pressure peak, and the ensuing relaxation of the IAS is compensated by a prompt perception of rectal distention and a concomitant contraction of the EAS until the rectum sufficiently relaxes to accommodate the distention. When used in incontinent patients, the rapid intermittent distention of a rectal balloon tests the ability of the anal sphincter to respond to rapid entry of feces into the rectum. A different situation exists during ramp inflation. At low rates of distention, the IAS often did not relax at all even when volumes of 250 mL had been infused into the rectal balloon. This suggests that, providing the entry of fecal material is sufficiently slow, continence may be maintained by the continued tone of the IAS, which maintains a pressure barrier between the rectum and the external environment when associated with the receptive relaxation of rectal tone. As distention proceeded at slow rates, the IAS tone was augmented by an increase in EAS activity that occurred when sensation was perceived. At higher rates of ramp distention, many subjects demonstrated anal relaxation at volumes that could not be perceived. Under these conditions, continence is severely threatened and could only be maintained by the residual activity in the EAS and IAS. In conclusion, the results obtained from this study show that sensory and reflex responses to rectal distention vary markedly according to the rate and pattern of the distention. They also suggest that these variations in responses may depend on activation of different populations of mechanoreceptors as well as modulation by rectal motor responses. Direct comparison of results from different centers is impossible unless the distention rate and characteristics of the balloon are identical. References 1. Schuster
MM, Hendrix TR, Mendeloff AI. The internal anal sphincter response: menometric studies on its normal physiology neural pathways and alteration in bowel disorders. J Clin Invest 1963;42:196-207. 2. Sun WM, Read NW. Anorectal function in normal human subjects: the effect of gender. Int J Colorectal Dis 1989;4:188-196.
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3. Ihre T. Studies on anal functions in continent and incontinent patients. Stand J Gastroenterol1974;9(Suppl25). 4. Buser WD, Miner PB Jr. Delayed rectal sensation with faecal incontinence, successful treatment using anorectal manometry. Gastroenterology 1986;91:1186-1191. 5. Wald A, Tunuguntla AK. Anorectal sensorimotor dysfunction in fecal incontinence and diabetes mellitus. N Engl J Med 1984;310: 1282-1287. 8. Behar J, Biancani P. Rectal function in patients with idiopathic chronic constipation. In: Roman C, ed. Gastrointestinal motility. London: MTP Press, 1984;459-466. 7. Kerrigan DD, Lucas MG, Sun WM, Donnelly TC, Read NW. Idiopathic constipation associated with impaired urethrovesical and sacral reflex function. Br J Surg 1989;76:748-751. 8. Porter NH. Megacolon: a physiological study. Proc R Sot Med 1961;54:1043-1047. 9. Callaghan RP, Nixon HH. Megarectum: physiological observations. Arch Dis Child 1964;39:153-157. 10. Caruana BJ, Hinds JP, Eidelman BH, Wald A. Anorectal sensorimotor dysfunction in multiple sclerosis and fecal incontinence: comparison with diabetes mellitus and fecal incontinence (abstr). Gastroenterology 1989;96:A75. 11. Read NW, Abouzekry L, Read MG. Howell P, Ottewell D. Donnelly TC. Anorectal function in elderly patients with fecal impaction. Gastroenterology 1985;89:959-966. 12. Rao SSC, Davison PA, Bannister JJ, Holdsworth CD, Read NW. Anorectal sensitivity and reactivity in patients with ulcerative colitis. Gastroenterology 1987;93:1270-1275. 13. Farthing MJG, Lennard-Jones JE. Sensibility of the rectum to distension and the ano-rectal distension reflex in ulcerative colitis. Gut 1978;19:64-69. 14. Sun WM. Read NW, Donnelly TC, Bannister JJ, Shorthouse AJ.
15. 16.
17. 18.
19.
20. 21.
22. 23.
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A common pathophysiology for full thickness rectal prolapse, anterior mucosa prolapse and solitary ulcer. Br J Surg 1989;76: 290-295. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable bowel syndrome. Gut 1973;14:125-132. Keighley MRB, Henry MM, Bartolo DCC. Mortensen NJMcC. Anorectal physiology measurement: report of a working party. Br J Surg 1989;76:358-357. Iggo A. Tension receptors in the stomach and the urinary bladder. J Physiol1955;128:593-607. Blumberg H, Haupt P, Janig W, Kohler W. Encoding of visceral noxious stimuli in the discharge patterns of visceral afferent fibres from the colon. Pflugers Arch 1983;398:33-40. Morrison JFB. Splanchnic slowly-adapting mechanoreceptors with punctate receptive fields in the mesentery and gastrointestinal tract of the cat. J Physiol1973;233:349-361. Basmajian JV, Stecko G. A new bipolar electrode for electromyagraphy. J Appl Physiol1962;17:849. Haynes WG. Read NW. Anorectal activity in man during rectal infusion of saline, a dynamic assessment of the anal continence mechanism. J Physiol1982;330:45-56. Varma JS, Smith AN. Reproducibility of the proctometrogram. Gut 1986;27:288-292. Clifton GL. Coggeshall Re, Vance WH, Willis WD. Receptive fields of unmyelinated ventral root afferent fibres in the cat. J Physiol1976;256:573-600.
Received January 23,199O. Accepted April 16,199O. Address requests for reprints to: Professor N. W. Read, Subdepartment of Gastrointestinal Physiology and Nutrition, Floor K, Royal Hallamshire Hospital, Sheffield SlO 2JF, England.
1990;99:1009-1015
Sensory and Motor Responses to Rectal Distention Vary According to Rate and Pattern of Balloon Inflation WE1 MING SUN, NICHOLAS W. READ, ALISON JO-ANNE DALY, S. KEVIN CHEAH, and DAVID Subdepartment of Gastrointestinal Sheffield, England
PRIOR, GRUNDY
Physiology and Nutrition, Royal Hallamshire
Anorectal motor activity and rectal sensation were recorded in 12 normal male subjects during ramp distention of the rectum with water and air at randomized rates of l&20, 50, and 100 mL/min and during intermittent rapid distention with air. There were no significant differences between the results of ramp inflation with water or with air, and the repeated infusion of the same medium yielded reproducible results. Ramp distention induced sigmoid pressure-volume profiles. Different sensations occurred at specific points on the pressure-volume curve and were maintained until succeeded by the next sensation. Initial perception of the distention occurred during the initial steep pressure increase, the sensation of wind occurred during the plateau phase, and the desire to defecate occurred at the onset of the final rapid ascent. Rectal sensations were induced at lower volumes at low infusion rates when the slope of the pressure-volume relationship was shallower than at high infusion rates. This suggests that the receptor triggering rectal sensation is not a simple volume or pressure receptor, but is more likely to be a slowly adapting mechanoreceptor lying parallel to the circular muscle of the rectal wall. During rapid intermittent distention, the rectal volumes required to elicit rectal sensations were lower than during ramp distention, although the pressure-volume curve was steeper. Moreover, sensations often only lasted a short period of time but recurred on deflation. These data suggest activation of an additional population of rapidly adapting or high threshold mechanoreceptors. Anal relaxation was always evoked by intermittent rectal distention and was almost always associated with a rectal sensation and an increase in external anal sphincter activity. In contrast, anal relaxation could be absent or delayed during ramp inflation, especially at lower infusion rates, suggesting that internal sphincter can
Hospital,
maintain continence for a long period of time while the rectum is slowly filling. Rectal sensation and concomitant external anal sphincter activity was not associated with anal relaxation during ramp inflation; most subjects felt the sensation long after the pressure reached its lowest level. However, under all circumstances the onset of rectal sensation was associated with an increase of external anal sphincter electrical activity. In conclusion, the rectal sensory and anorectal motor responses to distention depend on the rate and pattern of distention, which may activate a different population of receptors. Results from different laboratories cannot be compared directly unless the pattern and rate of distention are the same.
alloon distention of the rectum is an accepted simple method of measuring rectal compliance and evoking rectal sensation and reflex activity of the anal sphincter (1,2). Abnormal responses to balloon distention have been reported in patients with incontinence (3,4), diabetes mellitus (5), constipation (6,7), megacolon (8,9), multiple sclerosis (lo), fecal incontinence (in elderly patients) (ll), colitis (12,13), solitary ulcer syndrome (14), and irritable bowel syndrome (151, but results from different centers show a wide degree of variation which is generally thought to be related to differences in methodology. Different groups use balloons that are of differing shapes and sizes, inflate with different materials [air or water], use differing types of distention (ramp inflation at a continuous constant rate of infusion, stepwise increments,
B
Abbreviations used in this paper: EM, external anal sphincter; IAS, internal anal sphincter; MI, motility index. 0 1990 by the American Gastroenterological Association 0016-5035/90/s3.00
October 1990
intermittent distention with different volumes) and differing rates of inflation, and record responses in different ways. In a recent workshop (16), it was recommended that ramp inflation of the rectum would provide the most useful method to elicit sensory and motor responses because the rate of distention can be easily controlled. Does ramp distention test the same aspects of anorectal function as intermittent distention, and is the rate of rectal distention an important variable? No systematic study has been performed to answer these questions. It is commonly assumed that rectal distention elicits sensory and motor responses by triggering sensory receptors in the rectum or pelvic floor muscles. The precise nature of these receptors is not known. The rectum receives a dual afferent supply from the pelvic and lumbar splanchnic nerves. Electrophysiological studies in experimental animals have identified different populations of rectal mechanoreceptors that respond to distention and/or contraction and show a range of thresholds, firing rates, and rates of adaptation (17-19). Some respond to rapid changes and accommodate quickly to the new steady state and others respond to a more gradual change and continue to fire for long periods as the stimulus is maintained (18,191. It seems likely that both may coexist in the rectum and may show differential responses according to the rate of distention. The purpose of this study was to investigate how anorectal responses to rectal distention varied according to the pattern and rate of distention and also to the nature of the distending medium. The data provide some interesting insights into the nature of the rectal receptor mechanisms. Materials and Methods Subjects Twelve normal male volunteers (aged 20-25 years: median age, 22 years] who had no history of bowel disease were studied. A written consent form was obtained for the test to be performed. The protocol was approved by the Ethical Subcommittee of the Sheffield Health Authority in June 1988. Studies were performed at the same time of the day on three occasions separated by at least 1 week. No bowel preparation was used although subjects were encouraged to empty the rectum before the test if they felt the need to do so, and a digital examination of the rectum was performed immediately before the test to ensure that the rectum was empty.
Methods The subjects were lying in the left lateral position with the hips flexed to a go-degree angle, and a manometric probe consisting of a polyvinyl 7-lumen tube with an
VARIABLE
RESPONSES
TO RECTAL DISTENTION
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external diameter of 4 mm was inserted into the rectum. When correctly positioned, manometric side holes were situated in the anal canal at approximately 0.5, 1.0, and 2.0 cm from the anal verge and in the rectum at 4.5 and 15 cm. The side holes were perfused with water at a rate of 0.4 mL/min by a low-compliance pressurized perfusion system (Mui, PIP 2, Mississauga, Ontario, Canada], and pressures were measured by pressure transducers (Statham 23ID, Oxnard, CA) that were situated in each perfusion line and connected by means of amplifiers to a multichannel chart recorder (Hewlett Packard 7758A, Waltham, MA]. A highly compliant, thin-walled balloon constructed from a 6-cm cylinder (diameter = 5 cm] of unstretched condom (Durex Dry; LRC Products Ltd., London, England] was tied to the probe 5-11 cm from the anal verge. The pressure within the balloon was measured by a water-filled, nonperfused catheter connected to a transducer. The electrical activity of the sphincter was recorded using bipolar electrodes consisting of two trimel-coated wires (diameter, 0.025 mm) with their ends bared, hooked, and offset to avoid electrical contact (20.21). Two pairs of electrodes were inserted with the aid of a hypodermic needle, one into the superficial external anal sphincter (EAS) and the other into the internal anal sphincter (IAS). The EAS electrode was attached to an amplifier (differential type 2lCOl; URO-DISA, Copenhagen, Denmark), which was connected by means of an integrator (AC to RMS convertor; Analog Devices AD536,170 ms time constant, East Molesey, England) to the chart recorder. The IAS electrode was connected to the chart recorder by means of an amplifier (filter, 0.5-10 Hz). The activity of the IAS was represented on the raw electromyograph record as a regular oscillation which occured at a frequency of between 10 and 24 oscillations per minute and increased in amplitude as the activity of the muscle increased and vice versa. The integrated activity of the EAS was represented as an elevation above the base line.
Protocol Anorectal pressures were recorded under resting conditions for 20 minutes until they reached a steady state. Rectal distention was then performed. Each subject had 11 rectal distentions performed at three sessions. The balloon was inflated with air at a constant rate of 10, 20, 50, and 100 mL/min by means of a nitrogen gas cylinder equipped with a regulator or was inflated with water at the same rates by means of a peristaltic pump (Minipuls 3, Gilson 312, Villiers Le Bel, France]. The order of the ramp inflations was randomized. Both water and air were infused at room temperature. Inflation with water at the rate of 10 and 20 mL/min was performed on two separate occasions to test the reproducibility of the results. In each case, distention would continue until the subject complained of discomfort, and a gap of at least 20 minutes was allowed between inflations. Intermittent rapid distention of the rectum was performed by inflating the balloon at a rate of about 40 mL/s with volumes of 10, 20, 40, 60, and 100 mL of air by means of a handheld syringe. Each inflation was maintained .for 1 minute, then the balloon was deflated and a gap of at least 1 minute was allowed before the next inflation.
1010 SUN ET AL.
GASTROENTEROLOGY Vol. 99,No. 4
During rectal distention, subjects were instructed to report their initial perception, to report the onset of a feeling of gas in the rectum [wind) and the desire to defecate, and to indicate the onset and the duration of the sensation on the chart using a remote event marker. The lowest distending volumes at which the balloon was perceived and the lowest volumes required to induce a feeling of wind, a sensation of desire to defecate, and a sensation of discomfort or pain were recorded. The pressure-volume characteristics of the balloon at different rates of infusion of air and water were tested ex vivo before the start of each test. Those values were subtracted from the graph relating rectal balloon pressure and volume to yield values for rectal pressure at each distending volume. From these profiles, the slope of the rectal pressure and volume relationship was measured, and values for rectal compliance (dV/dP, mL/cm H,O) from 0 to 100 mL were also calculated. The motility index [MI) during balloon distention was expressed as the area under the manometry record from the rectal side-opening port.
Statistical
mL/min but was near the top at 100 mL/min (Figure 1). The perception of the sensation of wind occurred during the plateau phase and lasted while the pressure remained steady. The change in slope to the final rapid ascent was associated with the perception of a desire to defecate [Figure 1) and pain and discomfort was perceived during this final rapid ascent. The pressures for a given increment of volume were significantly lower (P < 0.05) at lower infusion rates (Figure 2). Thus the rectum was more compliant at a lower infusion rate than at a higher infusion rate [Figure 2). However, each sensation was perceived at lower volumes and at lower pressures when the infusion rate was slower (Tables 1 and 2) (Figure 1). Each different sensation was continuous until it was superceded by a new sensation. The lowest volumes required to cause rectal sensation, the sensation of wind, the desire to defecate, and discomfort were similar during either air or water infusion [Table 1). Moreover, the rectal pressures recorded at each particular rectal sensation [Table 2), the initial slope of the pressure increase, and the rectal compliance at each infusion rate did not show any significant differences between distention with water and distention with air (Figure 2). Repeated rectal distention with water at 10 and 20 mL/min showed similar results for rectal compliance (r = 0.62) and volumes and pressure for which initial perception (r = 0.91), desire to defecate (r = 0.931, and discomfort (r = 0.79) were perceived [Figure 3). The pressurevolume characteristics of the balloon were identical at the four infusion rates and irrespective of whether air or water was being infused (r > 0.99). Inflation of 50 mL of either air or water increased pressure by approximately 22 cm H,O; increasing volumes up to 300 mL caused no further pressure increments. Recordings from rectal side-opening ports. The pressures recorded in the rectal side holes increased as the distending volume increased. This pressure
Analysis
The statistical significance of the differences was determined by the F test. The correlation between the different treatments was examined by Pearson’s r test. The x2 test was used to analyze the percentage of subjects who showed certain phenomena at different rates of inflation.
Results Ramp
Inflation
Rectal pressure-volume relationship. The pressure-volume relationship during ramp inflations had a characteristic triphasic curve irrespective of the rate of inflation. This consisted of an initial steep increase followed by a plateau and a final rapid ascent [Figure 1). Different rectal sensations were perceived at different points on the curves. Initial perception of the distention occurred at the middle part of the steep aspect of the pressure increase at rates of 10.20, and 50
0
/
A
1.’ ,’ ,.,’
,I.’
5b Distension
volume
(ml)
100
150
200
Figure 1. Pressure-volume characteristics (A)during rectal ramp inflation with water at the rates of 10 (-+ 20 (-), 50 (-), and loo (. . . . .) mL/min and, (B) at the intermittent distention (- . . -1 with air. Data are the mean values of each distention. Arrows indicate where perception of the ballaon ( I), feeling of wind ( f ), and desire to defecate ( j ) I were felt.
VARIABLE RESPONSES TO RECTAL DISTENTION
October 1990
ab
a
1 a
ab
abc
defecate and discomfort were felt. These rapid increases were associated with repetitive contractions (Figure 4). The amplitude of rectal contractions was greater at higher infusion rates. However, when the motility indices were normalized to the same increments of volume, there were no significant differences (P > 0.05) between the different rates of infusion (Table 2). Motility indices during infusion of air and water at the same rates were also very similar. Anal responses. Fifty-eight percent of subjects showed no anal relaxation at all when the inflation rate was 10 mL/min, and 17% showed no relaxation at an inflation rate of 20 mL/min (P < 0.05 compared with 10 mL/min). All subjects showed anal relaxation at the inflation rates of 50 and 100 mL/min (P < 0.001 compared with 10 mL/min). Thirty-three percent of subjects showed anal relaxation within 3 seconds of the onset of the inflation at the inflation rates of 50 and 100 mL/min, 25% at 20 mL/min, and 17% at 10 mL/min. When relaxation occurred, the average delay in onset of relaxation was 68 + 2 seconds at 10 mL/min (P < 0.05 compared with 20, 50, and 100 mL/min), 35 c 10 seconds at 20 mL/min (P < 0.02 compared with 50 and 100 mL/min), 14 f 4 seconds at 50 mL/min (P < 0.05 compared with 100 mL/min), and 7 f 2 seconds at 100 mL/min. Anal relaxation was always associated with diminution of the amplitude of the IAS slow wave. At an infusion rate of 10 mL/min, five subjects perceived the balloon before the anal relaxation occurred, three at 20 mL/min and two at 50 mL/min. The rest of the subjects did not feel the sensation until long after the anal pressures reached the lowest steady state. None of the sensations occurred as the anus relaxed. The electrical activity of the EAS remained at basal levels as long as distention had not been perceived. Perception of the balloon was associated with an increase in the electrical activity of the EAS, and the
abed
1 a bc
I abed
1
I
100 intermittent
Perfusion
rate
1011
( mllmin)
Figure 2. Relationships between different perfusion rates and (A) theinitial slope of the rectal pressure increase and (B) the rectal compliance at the rectal volume of 100 mL The results obtained from water @) and air ( ?) ? inflation were compared. “Signi5cantly different than 10 mL/min, bsigni8cantly different than 20 mL/min, %ignificantly different than 50 mL/min, and dsigni5cantly different than 100 mL/min (P < 0.05). For intermittent rapid dietenHan, the steady-state pressure was plotted.
was greater in the high rectum (15 cm) than in the lower rectum (4.5 cm] [Figure 4). The pressure increase was gradual at first but increased rapidly just before (t5 seconds] or at the same time as the desire to
increase
Table 1. Comparison of the Lowest Rectal Volumes Required to Elicit Rectal Sensations Between Ramp Distention at Different Rates and Rapid Intermittent
Distention Inflation rate (mL/min] 20
10
Rectal volume (mL) Perception Wind Desire to defecate Discomfort
Water
Air
15 f 4 40 f 3 118 + 15 160 * 14
15 * 4 42 + 4 120 * 14 163 * 17
NOTE. Data are expressed “Significantly different from bSignificantly different from “Significantly different from dSignificantly different from
as mean * SEM. 10 mL/min. 20 mL/min. 50 mL/min. 100 mL/min.
Water 20 f 50 f 130 f 178 f
6 10 12 20
50 Air 20 + 5" 51 * 9" 128 f 10" 178 + 20’
Water 24 + 64 f 160 f 199 *
6 10 19 24
100 Air 22 *4"b 62 +9* 158 * 8& 210 zt 24*
Water 40 ilO 80 f 11 175 + 10 216 i 20
Air
Intermittent Air
43 * 1o*b" 12 * l"bCd 81 + gab= 27 + 4*cd 167 2 7&" 75 f 10*Cd 230 * 21&” 110 * lo&cd
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1012 SUN ET AL.
Table 2. Comparison of the Lowest Rectal Pressures Associated With Rectal Sensations Between
Ramp Distention
at Different
Rates and Rapid
Intermittent
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and the Rectal Motility Indices
Distention
Inflation rate (mL/min) IO
Rectal pressure (cm H,O) Sensation Wind Desire to defecate Discomfort Motility index (mm”/min) NOTE. Data “Significantly bSignificantly “Significantly dSignificantly
20
100
50
Water
Air
Water
Air
Water
7*1 IO + 3 13 * 2 18 f 2 61 + 20
7&l 11 f 4 14 k 2 18 zt2 62 f 20
IO + 2 15 + 2 18 i:2 22 + 3 71 k 25
11 km2" 14 f 3O 19 f 2O 22 + 4" 75 * 25
13 + 2 17 * 3 22 f 3 30 + 4 70 f 25
Air
13 *1* 16 t 3* 22 + 3"b 33 *4* 80 k 23
Water
Air
18 + 3 22 f 2 29 * 4 36 f 5 100 i 30
1922h 21 + 1*c 28 + 4&' 38 k 70bc 98 f 30
Intermittent Air 13 f l*d 21 + 3"bc 30 f 3"bc 37 k 5"h"
are expressed as mean * SEM. different from IOmL/min. different from 20 mL/min. different from 50 mL/min. different from 100 mL/min.
increase was maintained or enhanced as the infusion volume increased (Figure 4). The onset of each new sensation was associated with a burst of EAS electrical activity (Figure 4). Intermittent
Distention
Rectal responses and sensation. Intermittent balloon inflation with increasing volumes of air was associated with an initial increase in pressure in the rectal balloon as the air was introduced. This was often followed by a transient secondary increase in pressure. The pressure then gradually subsided to a steady state. Rectal pressure increased in amplitude and duration as the distending volume increased. The
. .
Discomfort
DD
Perception rz0.96
pressure changes for given pressure increments were significantly greater during intermittent distention (P < 0.05) than during ramp inflations (Figure l), and rectal compliance was consequently much lower (P < 0.05) during intermittent distention (Figure 1). The pressures recorded by the rectal side holes showed components similar to those in the balloon channel. Repetitive rectal contractions were seen in the rectal channels when the desire to defecate was experienced. The amplitude of contractions was larger in the upper rectal channel than in the lower rectal channel. The relationship between steady-state pressure and volume during intermittent distention also consisted of three components: an initial rapid increase, a slower increase, and a final rapid ascent. Rectal
rc0.93
200
.
.
. .
r zO.82
300
.’. . ..
0
50 Rectal
volume
r-=0.96
50 1
50
. *. ‘.
. a.
.
.
. .
50
0
20 Rectal
pressure (2nd
*.- . .
300
(ml)
(2nd value)
rz0.91
.
(cm H20)
value)
.; * . .L. %. r=0.79
0
50
Figure 3. Diagram to illustrate (A) the reproducibility of the repeated measurements of rectal volume required to elicit rectal sensation end (B) the rectal pressures required to elicit different rectal sensation at the inflation rate of 20 mL/min.
October
VARIABLE
1990
Channel
c”lzO 320
1
l----
0
60 6 0
-
I
I ntogated EMG
k
t felt
wind
tt
dd discor%
RESPONSES TO RECTAL DISTENTION
1013
decline in anal pressure that was usually observed in all anal channels and was associated with the suppression of IAS electrical oscillations. All subjects showed anal relaxation at a distending volume of 10 mL (compared with 5 of 12 during 10 mL/min ramp inflation: P -C0.001). As the rectal volume increased, the electrical activity of the EAS increased in amplitude and duration, while the anal pressure decreased in amplitude and increased in duration. The EAS activity was tightly linked to perception during intermittent rectal distention. Two subjects, who did not feel the distention with 10 mL of air, did not show any electrical activity of the EAS. Similarly, subjects did not perceive the sensation if the distention did not elicit rectal contraction. The duration of rectal contraction, rectal sensation, and EAS activity were closely related (r > 0.8). Upon deflation of the balloon, the anal pressure often increased to values that were higher than the preinflation pressures. The rebound increases in pressure lasted at least 1 minute when rectal volumes exceeded 60 mL and were always associated with increases in the amplitude of the IAS slow wave.
.)
Figure 4.
Recordings of anorectal pressures at ports
situated at 0.5,
and 15 cm from the anal verge and in the rectal balloon (5-11 cm from the anal margin) [channels l-6)and the integrated electrical activity of EAS(channel7] during ramp inflation with air at the rate of 50 mL/min. Note that (a) the rectal pressures increased during the rectal inflation and the pressures recorded at higher rectal channels are higher than at lower ones, (b) the rectal pressures increased when desire to defecate (da) and discomfort were felt, and (c] an increase in electrical activity of the EAS was associated with the onset of each specific rectal sensation. 1.0,2.0,4.5,
sensation was perceived during the initial rapid increase, a sensation of wind was felt at the beginning of the slow increase (presumably corresponding to the plateau during ramp inflation), and the desire to defecate was experienced when the pressure started to climb steeply again. Despite the lower compliance, the rectal distending volumes required to elicit rectal sensations were significantly lower (P < 0.001) during intermittent distention (Table 1). All subjects felt a rectal sensation during inflation at 20 mL, and all except two subjects perceived the balloon at 10 mL. At low volumes, a transient sensation was experienced as the balloon was inflated, and a similar transient sensation was perceived as the balloon was deflated. The sensation became more prolonged as the distention volume increased. Anal responses. Intermittent distention of the rectal balloon caused a transient increase in anal pressure, seen most clearly in the outermost anal channels and associated with an increase in the electrical activity of the EAS. This was followed by a
Discussion The results of this study show that the sensory and motor responses of the rectal distention are affected by the rate and pattern of distention but not by the change of medium (water or air). Repetitive distention at the same rate shows a high degree of reproducibility, as previously reported by Varma and Smith (22). Ramp inflation generates a sigmoid pressure profile. The early rapid increase presumably reflects the elastic properties of the tonically contracted bowel and ends in a plateau phase, presumably when the distending stimulus induces receptive relaxation. The final increase occurs at the limits of relaxation and represents the elastic properties of the relaxed bowel. Irrespective of the rate of distention, the sensory experiences of rectal distention, which range from sensation of wind to desire to defecate to discomfort, are closely associated with the rectal pressure profiles observed during distention. Initial sensation was first experienced during the initial rapid increase in pressure. A feeling of “wind” occurred near the beginning of the plateau when the rectum was relaxing to accommodate the increasing volume, while a desire to defecate occurred when the rectum reached its limit of accommodation and pressure began to increase steeply again. Rectal sensation and anorectal motor responses varied according to the rate of ramp inflation. Increasing the rate of inflation produced graded increases in pressure at each volume, suggesting that the time-
1014
SUN ET AL.
dependent relaxation of rectal smooth muscle is overcome at higher flow rates. Moreover, rectal sensations were perceived at lower volumes when the infusion rate was slower and pressures were lower. These results are incompatible with a simple volume or pressure receptor; instead they suggest the activation of a slowly adapting mechanoreceptor within or on the rectal wall. Such a receptor would be subjected to a greater degree of stimulation when the rectum relaxes; relaxation occurs earlier and at lower volumes when infusion rate is slowest. This arrangement is facilitated by the tubular nature of the rectum. When lateral expansion of the balloon is limited by tonic contraction of rectal smooth muscle, the balloon can still extend in a longitudinal direction. In this way, rectal receptors are protected from circumferential stretch at high rates of distention and a greater rectal volume can be tolerated. The facility for longitudinal extension of the balloon would also explain why distention with a compressible gas yields results that are virtually identical to those obtained when the rectum is distended with a less compressible liquid. Rectal sensations were perceived at much lower volumes during intermittent rapid distention of the rectum than during ramp inflation. However, at low volumes the sensations did not last for the duration of the distention. One possible interpretation is that rapid distention stimulates an additional population of rapidly adapting mechanoreceptors. If this is correct, then the perception of a transient sensation when the balloon is both inflated and deflated is compatible with the behavior of mucosal receptors stimulated by the rapidly expanding or contracting balloon (23). An alternative interpretation is that intermittent distention activates a high threshold receptor, which only fires at the initial peak in rectal pressure that occurs as the balloon is inflated. In this regard, we have previously described a close correlation between the duration of transient peak in rectal pressure induced by rapid intermittent distention and the duration of sensation (2). It is perhaps simplistic to presume that rectal perception is induced by activation of a single population of mechanoreceptors. It is likely that the final conscious perceptions of rectal distention arise from a combination of sensory inputs with reflex responses to the distention modulating the sensory experience. Sensation may be modulated, for example, by the changes in rectal compliance observed at different rates of distention, stimulation of mucosal receptors, and activation of receptors in the high rectum or sigmoid colon caused by longitudinal extension of the balloon. In this study, the urge to defecate was associated with increased contractile activity in the proximal pressure port. However, there was no temporal relationship
GASTROENTEROLOGY
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between rectal sensation and the onset of anal relaxation. There are also important differences between the anal responses to intermittent and ramp distention of the rectum, and these may also relate to activation of different populations of receptors. Intermittent distention induced a prompt relaxation of the IAS and a contraction of the EAS that was closely associated with sensation and always occurred at volumes that were equal to or lower than those that elicited anal relaxation. Thus the threat to continence produced by rapid entry of fecal material into the rectum, the high rectal pressure peak, and the ensuing relaxation of the IAS is compensated by a prompt perception of rectal distention and a concomitant contraction of the EAS until the rectum sufficiently relaxes to accommodate the distention. When used in incontinent patients, the rapid intermittent distention of a rectal balloon tests the ability of the anal sphincter to respond to rapid entry of feces into the rectum. A different situation exists during ramp inflation. At low rates of distention, the IAS often did not relax at all even when volumes of 250 mL had been infused into the rectal balloon. This suggests that, providing the entry of fecal material is sufficiently slow, continence may be maintained by the continued tone of the IAS, which maintains a pressure barrier between the rectum and the external environment when associated with the receptive relaxation of rectal tone. As distention proceeded at slow rates, the IAS tone was augmented by an increase in EAS activity that occurred when sensation was perceived. At higher rates of ramp distention, many subjects demonstrated anal relaxation at volumes that could not be perceived. Under these conditions, continence is severely threatened and could only be maintained by the residual activity in the EAS and IAS. In conclusion, the results obtained from this study show that sensory and reflex responses to rectal distention vary markedly according to the rate and pattern of the distention. They also suggest that these variations in responses may depend on activation of different populations of mechanoreceptors as well as modulation by rectal motor responses. Direct comparison of results from different centers is impossible unless the distention rate and characteristics of the balloon are identical. References 1. Schuster
MM, Hendrix TR, Mendeloff AI. The internal anal sphincter response: menometric studies on its normal physiology neural pathways and alteration in bowel disorders. J Clin Invest 1963;42:196-207. 2. Sun WM, Read NW. Anorectal function in normal human subjects: the effect of gender. Int J Colorectal Dis 1989;4:188-196.
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3. Ihre T. Studies on anal functions in continent and incontinent patients. Stand J Gastroenterol1974;9(Suppl25). 4. Buser WD, Miner PB Jr. Delayed rectal sensation with faecal incontinence, successful treatment using anorectal manometry. Gastroenterology 1986;91:1186-1191. 5. Wald A, Tunuguntla AK. Anorectal sensorimotor dysfunction in fecal incontinence and diabetes mellitus. N Engl J Med 1984;310: 1282-1287. 8. Behar J, Biancani P. Rectal function in patients with idiopathic chronic constipation. In: Roman C, ed. Gastrointestinal motility. London: MTP Press, 1984;459-466. 7. Kerrigan DD, Lucas MG, Sun WM, Donnelly TC, Read NW. Idiopathic constipation associated with impaired urethrovesical and sacral reflex function. Br J Surg 1989;76:748-751. 8. Porter NH. Megacolon: a physiological study. Proc R Sot Med 1961;54:1043-1047. 9. Callaghan RP, Nixon HH. Megarectum: physiological observations. Arch Dis Child 1964;39:153-157. 10. Caruana BJ, Hinds JP, Eidelman BH, Wald A. Anorectal sensorimotor dysfunction in multiple sclerosis and fecal incontinence: comparison with diabetes mellitus and fecal incontinence (abstr). Gastroenterology 1989;96:A75. 11. Read NW, Abouzekry L, Read MG. Howell P, Ottewell D. Donnelly TC. Anorectal function in elderly patients with fecal impaction. Gastroenterology 1985;89:959-966. 12. Rao SSC, Davison PA, Bannister JJ, Holdsworth CD, Read NW. Anorectal sensitivity and reactivity in patients with ulcerative colitis. Gastroenterology 1987;93:1270-1275. 13. Farthing MJG, Lennard-Jones JE. Sensibility of the rectum to distension and the ano-rectal distension reflex in ulcerative colitis. Gut 1978;19:64-69. 14. Sun WM. Read NW, Donnelly TC, Bannister JJ, Shorthouse AJ.
15. 16.
17. 18.
19.
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22. 23.
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A common pathophysiology for full thickness rectal prolapse, anterior mucosa prolapse and solitary ulcer. Br J Surg 1989;76: 290-295. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable bowel syndrome. Gut 1973;14:125-132. Keighley MRB, Henry MM, Bartolo DCC. Mortensen NJMcC. Anorectal physiology measurement: report of a working party. Br J Surg 1989;76:358-357. Iggo A. Tension receptors in the stomach and the urinary bladder. J Physiol1955;128:593-607. Blumberg H, Haupt P, Janig W, Kohler W. Encoding of visceral noxious stimuli in the discharge patterns of visceral afferent fibres from the colon. Pflugers Arch 1983;398:33-40. Morrison JFB. Splanchnic slowly-adapting mechanoreceptors with punctate receptive fields in the mesentery and gastrointestinal tract of the cat. J Physiol1973;233:349-361. Basmajian JV, Stecko G. A new bipolar electrode for electromyagraphy. J Appl Physiol1962;17:849. Haynes WG. Read NW. Anorectal activity in man during rectal infusion of saline, a dynamic assessment of the anal continence mechanism. J Physiol1982;330:45-56. Varma JS, Smith AN. Reproducibility of the proctometrogram. Gut 1986;27:288-292. Clifton GL. Coggeshall Re, Vance WH, Willis WD. Receptive fields of unmyelinated ventral root afferent fibres in the cat. J Physiol1976;256:573-600.
Received January 23,199O. Accepted April 16,199O. Address requests for reprints to: Professor N. W. Read, Subdepartment of Gastrointestinal Physiology and Nutrition, Floor K, Royal Hallamshire Hospital, Sheffield SlO 2JF, England.
