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588 Fecal Continence Revisited: The Anal External Sphincter Continence Reflex [2013.11.DCR] 2013-12-17 3808

Fecal Continence Revisited: The Anal External Sphincter Continence Reflex

Broens, Paul M. A. M.D., Ph.D.1; Penninckx, Freddy M. M.D., Ph.D.2; Ochoa, José Boix M.D., Ph.D.3




Author Information

1 Department of Surgery, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands

2 Department of Abdominal Surgery, University Hospital Gasthuisberg, Catholic University of Leuven, Leuven, Belgium

3 Department of Pediatric Surgery, Hospital Infantil Valle d’Hebrón, Autonomous University, Barcelona, Spain

Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML and PDF versions of this article on the journal’s Web site (www.dcrjournal.com)

Financial Disclosure: None reported.

Correspondence: Paul M. A. Broens, M.D., Ph.D., Department of Surgery, Division of Pediatric Surgery, University Medical Center Groningen, P.O. Box 30 001, 9700 RB Groningen, the Netherlands. E-mail: p.m.a.broens@umcg.nl.


Abstract

BACKGROUND: None of the current theories on fecal incontinence can explain fecal continence adequately.

OBJECTIVE: This study aims to evaluate the mechanism controlling fecal continence.

DESIGN: Anal electrosensitivity, anorectal pressures, and rectal pressure volumetry tests were performed in 17 controls before and after superficial local anal anesthesia and in 6 controls before and after spinal anesthesia. The same tests were performed in 1 patient before and after injected local anal anesthesia and in 3 patients with spinal cord lesions at levels Th3 to L3.

RESULTS: After superficial local anal anesthesia, anal electrosensitivity decreased, but basal anal pressure remained unaltered. Squeeze pressure decreased and rectal filling sensation levels remained. Local anesthesia reduced anal pressure recorded in the distal anal canal during progressive rectal filling. This was also the case, albeit more explicit, after the local anal anesthetic was injected. After spinal anesthesia, the anal canal became insensitive to electric stimulation, but basal and squeeze pressure values decreased substantially, and the increase in anal pressure during the balloon-retaining test disappeared completely. In the patients with spinal cord lesions, the external sphincter could not be squeezed on command, but during the balloon-retaining test, the anal sphincter did squeeze autonomously at more than 300 mmHg.

LIMITATIONS: These were partially experimental measurements. The relevance of the found model in the daily clinical practice will have to be studied in a following study.

CONCLUSIONS: Our results support the hypothesis that the component of fecal continence mediated by contraction of the external sphincter depends on a anal external sphincter continence reflex without involving the brain. Presumably, the afferent receptors of this reflex are contact receptors located superficially in the mucosa or submucosa of the distal anal canal. A nonfunctioning anal external sphincter continence reflex would, therefore, result in fecal incontinence (see Video, Supplemental Digital Content 1, http://links.lww.com/DCR/A116).


Anorectal sensation, the sphincter barrier (internal anal sphincter and external anal sphincter), the anorectal angle (puborectal muscle), and the hemorrhoidal plexuses are the components of anorectal continence.

Different theories have been postulated to explain the mechanisms underlying fecal incontinence. First, the efferent neurogenic theory suggests that sustained nerve damage results in sphincter weakness.1 Second, the myogenic theory suggests structural sphincter damage resulting from vaginal delivery.2–4 Indeed, both types of abnormalities were reported in more than 90% of incontinent patients.3,5 Nevertheless, in 70% of patients, sphincter defects do not lead to incontinence,4,6 nor does classical neurophysiology of the anorectum (pudendal nerve motor latency time and single-fiber electromyography of the anal sphincter) correlate with symptoms.7,8 Other theories have explained fecal incontinence in terms of disturbed anorectal sensations.9–11

None of the above-mentioned theories, however, can explain why patients with mild sphincter damage can be severely incontinent, nor can they explain why some patients are incontinent only during sleep, nor why patients with traumatic spinal cord lesions lose larger amounts of stool once or twice during the day, instead of losing small amounts during the entire day.1–13 We propose a new, afferent neurogenic theory. It suggests that fecal continence is controlled by an autonomous spinal cord reflex, without involving the brain. Once the fecal mass is into the anal canal, it triggers mucosal or submucosal continence receptors in the anal canal that induce contraction of the external anal sphincter. We revisited the sensory side of fecal continence suggesting that topical anesthesia could abort continence mechanisms and mucosal sensitivity as a basis for a local spinal reflex. We tested this hypothesis by comparing the results of 3 rectal sensation tests – the anal electrosensitivity test, the rectoanal inhibitory reflex test, and the rectal filling sensation test – before and after applying a local anesthetic in the anal canal (superficial or injected), before and after spinal anesthesia, and in patients with spinal cord lesions.

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MATERIALS AND METHODS

Participants
Test Subjects

We performed the rectal sensation tests in 17 volunteer test subjects, mean age 56 (range, 26–83; 6 females, 11 males). Exclusion criteria were neurological and/or endocrine diseases, or a subjectively disordered anal function. We assessed the latter by a detailed questionnaire and anal manometry. Of these 17 subjects, 9 were tested before partial colonic resection for a right or left colon tumor and 8 were tested in the context of minor surgery (laparoscopic appendectomy, cholecystectomy, inguinal hernia, ventral incisional hernia repair).

We tested a second control group of 6 male patients, mean age 64 (SD, 18; range, 38–80), who underwent inguinal hernia surgery under spinal anesthesia, before and after surgery.

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Patients

We tested 1 male patient, aged 65, with chronic anal fissure, who underwent skin tag resection and lateral internal sphincterotomy under general anesthesia, before and after surgery. Finally, we tested 3 patients, aged 15, 17, and 18, with complete spinal cord lesions at levels L3, L3, and Th4.

All participants gave their informed consent

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Measuring Equipment

The data were collected and analyzed with Solar Gastrointestinal high-resolution manometry equipment (Medical Measurement Systems BV, Enschede, The Netherlands) using customized Unisensor solid state circumferential catheters and microtip pressure transducer catheters.

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Tests
Anal Electrosensitivity Test

This test determines the sensitivity of the anal canal.9 We noted the threshold values of the lowest perceptible stimulus intensity at 5 levels, starting at 1 cm above the anal verge, to assess the degree of anesthesia over the entire length of the anal canal.

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Anorectal Manometry

Anal manometry measures the strength of the anal sphincter at rest and during maximal squeeze.14

The rectoanal inhibitory reflex-test provides information about the inhibitory relaxation of the internal anal sphincter after dilatation of the rectum.14 We noted the distending volumes at which the first and the maximum anal relaxation was observed.

The rectal filling sensation test provides information about the patient’s ability to feel rectal filling and whether the anal canal reacts to rectal filling with squeeze as was demonstrated by us earlier.15–17 The test was performed with the patient sitting upright on a commode. The patient was instructed to retain the rectal balloon for as long as possible and to report the following sensations: first sensation, constant sensation, and urge sensation. The test was stopped when the patient reached maximum tolerable sensation, ie, when filling reached the limit of tolerance. If the patient was unable to retain the balloon until maximum tolerable sensation, we stopped recording as soon as the balloon left the anal canal and considered this to be the maximum retainable volume.

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Measuring Procedures

1. The subjects in the superficial local anal anesthesia group were first given the above-mentioned 3 tests. Subsequently, they were given a local anesthetic (9 g of lidocaine 2% jelly) on a surgical gauze inserted in the anal canal. In order not to influence the rectum, we seated the subjects upright immediately. After approximately 20 minutes, we removed the gauze and repeated the 3 tests.

2. The 1 patient injected with the local anal anesthetic was also first given the 3 tests before undergoing skin tag resection and lateral internal sphincterotomy under general anesthesia. After the operation had been performed, the patient’s anal subepithelium was circumferentially injected with 8 mL of lidocaine 1% and adrenaline 1:100,000, from the anal verge to 4 cm above it. We repeated the 3 tests 30 minutes after the operation, by which time the general anesthesia had worn off completely. Seven hours later, when the effect of the local anesthetic had disappeared subjectively, we tested the patient again for a third time.

3. The patients in the spinal anesthesia group were also given the 3 above-mentioned tests before being anesthetized for a surgical procedure. Subsequently, they received a spinal anesthetic. The level of spinal anesthesia, as measured by the anesthesiologist, ranged from level Th3 to Th6. Immediately after the surgery was completed, but while the spinal anesthetic was still fully effective, we repeated the 3 tests. Contrary to the other groups, we studied these patients while they were lying in the left lateral position (before and after spinal anesthesia), because they were unable to sit upright on a commode while still under the influence of the spinal anesthetic.

4. The 3 tests were performed only once in the patients with spinal cord lesions while they were seated upright on a commode.

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Statistical Analysis

We analyzed our data with SPSS for Windows, version 18.0 (IBM SPSS Statistics, IBM Corporation, Armonk, NY). Because we used nonparametric tests, we report median, minimum, and maximum values. We used the Wilcoxon test for paired data to compare the effect of the different types of anesthetics. A p value of ≤0.05 was considered significant. For correlation calculations, we used Spearman rank correlations.

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RESULTS

The Effect of Superficial Local Anal Anesthesia

After superficial local anal anesthesia, patients’ anal electrosensitivity decreased significantly at all levels (p < 0.001), in particular, at 2 cm, from 4 mA (range, 2–10) to 7 mA (range, 2–17); 3 cm, from 5 mA (range, 2 to >25) to 9 mA (range, 4 to >25); and 4 cm above the anal verge, from 9 mA (range, 2 to >25) to 25 mA (range, 6 to >25).

The maximal anal basal pressure as well as the length of the anal high pressure zone did not change. By contrast, squeeze pressure significantly decreased from 370 mmHg (range, 180–540) before anesthesia to 290 mmHg (range, 105–530) after anesthesia (p < 0.001).

The thresholds to induce the first rectoanal inhibitory reflex and the threshold to induce maximum internal sphincter relaxation were not influenced by superficial local anal anesthesia.

During progressive rectal filling, the proximal anal canal pressure increased significantly from constant sensation to maximum tolerable sensation (Table 1). After superficial local anal anesthesia, this proximal anal pressure increase was absent. Moreover, this type of anesthesia also significantly reduced the pressure in the distal anal canal at all sensation levels (Table 1).


TABLE 1. The effect of the superficial local anal anesthetic

After superficial local anal anesthesia, we observed that, of 17 patients, 2 were unconscious of losing the rectal balloon, although they had experienced first sensation, constant sensation, and urge sensation before involuntary evacuation. These 2 patients had markedly reduced distal anal pressure increase during rectal balloon filling (Fig. 1).


FIGURE 1. An example of a subject who involuntarily lost the rectal balloon after superficial local anal anesthesia. Left, The effect of the anal-external sphincter continence reflex. To preserve fecal continence the external sphincter contracts continuously for several minutes as soon as the first sensation level is reached. Right, The results of the same test with the same subject after applying the local anesthetic. The pressure in the distal anal canal could no longer be increased, and the subject was unable retain the rectal balloon despite experiencing the rectal filling sensations up to urge sensation. The rectal balloon volumes, pressures, and time from the beginning of the test up to the subsequent rectal filling sensations, are given. AESCR = anal-external sphincter continence reflex; FS = first sensation; CS = constant sensation; US = urge sensation; MTS = maximal tolerable sensation; MRV = maximal retainable volume.

Superficial local anal anesthesia did not affect all anal levels equally. We therefore explored the possibility of a correlation between the anal electrosensitivity and the proximal and distal anal canal pressure during progressive rectal filling sensations before and after local anesthesia. After superficial local anal anesthesia, we found a significant inverse correlation. The higher the stimulus needed to reach anal sensitivity in the distal anal canal, the lower the pressure in the anal canal.

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The Effect of Anal Mucosal or Submucosal Lidocaine Injection

In the patient who had been administered the mucosal or submucosal lidocaine injection, the anal epithelium became completely insensitive to electric stimulation at all levels. Maximum anal basal pressure decreased from 170 to 80 mmHg and squeeze pressure from 410 to 130 mmHg with recovery of both values after 7 hours, whereas anal electrosensitivity almost normalized after 7 hours (18, 3, 6, 7, and 6 mA at 5–1 cm above the anal verge).

The thresholds for first and maximum rectoanal inhibitory reflex were unaffected by this type of anesthetic. The distal anal pressures during the successive rectal filling sensations were strongly reduced (Fig. 2).


FIGURE 2. The effect of the injected local anal anesthetic on the rectal filling sensation test on the patient with chronic anal fissure. Left, Before applying the anesthetic, the anal pressure was significantly increased. Middle, The same patient after lateral sphincterotomy and anal submucosal injection of the local anesthetic. The high anal pressure normalized to normal values. The pressure and volumes necessary to elicit rectal filling sensations are significantly increased. Right, The same patient after a few hours when the local anesthetic had practically worn off. Anal pressure increases significantly once again. The pressure and volumes necessary to elicit rectal filling sensations are still increased but lower in comparison with the situation after the local anal anesthetic had been injected. The rectal balloon volumes, pressures, and time from the beginning of the test up to the subsequent rectal filling sensations are given. FS = first sensation; CS = constant sensation; US = urge sensation; MTS = maximal tolerable sensation.
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The Effect of Spinal Anesthesia

Spinal anesthesia resulted in a significant decrease of maximum anal basal pressure from 95 mmHg (range, 80–125) to 25 mmHg (range, 20–65), p < 0.05. Squeeze pressure was almost completely abolished and decreased from 440 mmHg (range, 230–500) to 35 mmHg (range, 30–80), p < 0.05. The anal canal became completely insensitive to electric stimulation up to 25 mA, and rectal filling sensations disappeared completely. In contrast, the thresholds for inducing the first and the maximum rectoanal inhibitory reflex were not affected.

The anal pressure increase that is normally observed during progressive rectal filling was completely absent after spinal anesthesia.

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Patients With Spinal Cord Lesions

The 3 patients with spinal cord lesions were unable to voluntarily squeeze the external sphincter, but they were able to retain the rectal balloon during the balloon retention test up to a volume of 155 mL by increasing the anal pressure. During the balloon retention test, however, the external sphincter did contract, increasing the anal pressure by more than 300 mmHg.

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DISCUSSION

In terms of the classic theory of fecal incontinence, as illustrated by Figure 3A, it is generally believed that fecal continence depends on the ability to feel the rectal filling sensation,18 whereupon the brain sends a stimulus to the external sphincter to contract and fecal continence is maintained.



FIGURE 3. A, Diagram of the classic fecal continence theory. Filling of the rectal balloon gives a rectal filling sensation by the rectal wall that sends a signal to the brain. The brain orders the external sphincter to contract, and, with that, fecal continence is maintained. Fecal continence depends, therefore, on awareness of the rectal filling sensation and on a brain-controlled contraction of the external sphincter. B, Diagram of our new fecal continence theory. Filling the rectal balloon makes it descend into the anal canal. There, the balloon activates the continence receptor to signal to the external sphincter to contract. This signal is connected directly to the external sphincter by a spinal reflex without involving the brain. Fecal continence is, therefore, independent of awareness of rectal filling sensation and depends directly on the anal-external sphincter continence reflex.
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Rectal Filling Sensation Is Not Directly Responsible for Fecal Continence

Figure 3B illustrates our theory of fecal continence. On the basis of our findings, we postulate that the rectal filling sensation is not directly responsible for fecal continence. Indeed, after superficial local anal anesthesia, the distal anal pressure was significantly lower in all 17 control subjects, and 2 of them even lost the rectal balloon involuntarily before reaching maximum tolerable sensation and were completely unaware of the fact. Although it has been assumed for a considerable length of time that fecal continence depends on rectal filling sensations, our observation that 2 people involuntarily lost the rectal balloon despite reporting all the normal rectal filling sensations, proves that continence does not depend directly on rectal filling sensation. Suppression of a continence reflex could explain why these subjects lost the rectal balloon despite the presence of a previous urge sensation.

In contrast, the patients with spinal cord lesions were able to retain the rectal balloon up to a volume of 155 mL by contracting the external sphincter, despite the fact that they were unable to sense normal rectal filling sensations. This observation reinforced our conclusion that fecal continence does not depend directly on the rectal filling sensation.

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The Anal Continence Reflex Is a Spinal Reflex

In the 6 subjects belonging to the spinal anesthesia group, whose spinal cords were blocked from level Th3 or Th6 down to S5, the normal increase of pressure during the rectal filling sensation test had disappeared. Obviously, as a consequence of spinal anesthesia, the anal continence reflex had disappeared completely. Following spinal cord lesions, which leave the spinal cord intact below the level of the lesion, the anal continence reflex remained present. This observation, therefore, led us to conclude that the anal continence reflex is a spinal reflex. The external sphincter can contract without involving the brain.

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Fecal Continence Under Normal Circumstances

Under normal physiological circumstances, the migration of fecal content into the anal canal sets off a reflex-induced external anal sphincter contraction. When this reflex reaches its maximum, ie, urge sensation, strong contractions alert the individual to the fact that he or she needs to urgently and voluntarily contract the external sphincter. By so doing, the fecal content is forced back into the rectum, thus avoiding involuntary loss of fecal content. (Fig. 4A). The brain may overrule the continence reflex by building up extra pressure in the abdomen and relaxation of the anal sphincter causing the fecal mass to be expelled (Fig. 4B, C).



FIGURE 4. Diagram representing the stages of fecal continence according to our theory. A, Fecal content high up in the rectum. The AESCR is at rest. B, Fecal content in the anal canal. The AESCR activates the external sphincter to contract, and, thus, fecal continence is controlled. This is a stable situation until urge sensation is reached. Then, 1 of 2 possibilities arise, either this status is supported by the brain and the fecal mass moves back up into the rectum, or the body overrules this status by increasing abdominal pressure and relaxing the external sphincter, causing the fecal mass to be expelled. C, After the fecal mass has been expelled the AESCR is again at rest. AESCR = anal-external sphincter continence reflex.


FIGURE 4. Diagram representing the stages of fecal continence according to our theory. A, Fecal content high up in the rectum. The AESCR is at rest. B, Fecal content in the anal canal. The AESCR activates the external sphincter to contract, and, thus, fecal continence is controlled. This is a stable situation until urge sensation is reached. Then, 1 of 2 possibilities arise, either this status is supported by the brain and the fecal mass moves back up into the rectum, or the body overrules this status by increasing abdominal pressure and relaxing the external sphincter, causing the fecal mass to be expelled. C, After the fecal mass has been expelled the AESCR is again at rest. AESCR = anal-external sphincter continence reflex.
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Fecal Continence by External Sphincter Contraction Is Controlled by Mucosal or Submucosal Anal Receptors

We found that superficial local anal anesthesia had no influence whatsoever on anal basal pressure. It did, however, result in a significant decrease of squeeze pressure, albeit sufficient for normal fecal continence.19–21 We also observed a significantly reduced increase of distal anal pressure during progressive rectal filling. The basal anal sphincter pressure did not alter under the influence of the topical anal anesthesia, but the force of contraction of the anal sphincter decreased significantly.

After lateral sphincterotomy and injection of a local anesthetic, anal basal pressure normalized in the patient with chronic anal fissure. After the local anesthetic had practically worn off and the subject’s anal electrosensibility had almost returned to normal, high basal pressure increased significantly, even though the internal sphincter could no longer be responsible for this increase.

These observations suggested the presence of a reflex that we named the anal-external sphincter continence reflex (AESCR) (Fig. 3B). Because the maximum anal squeeze pressure decreased significantly after applying the local anal anesthetic, these distal anal receptors seem also to be stimulated during squeeze to reinforce the voluntary external sphincter contraction.

The superficial local anal anesthetic can only influence the epithelium and the first millimeter or so below the epithelium, a fact that led us to assume that the continence receptor is located superficially in the mucosal or submucosal tissue (Fig. 3B).

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The Anal Continence Receptors Are Located in the Lower Anal Canal

After superficial local anal anesthesia, we found an inverse correlation between the anal canal electrosensitivity at 1 cm to 3 cm from the anal verge and the proximal anal canal pressure. These findings and the observation of numerous receptors in the anal canal by Duthie et al12 indicated the presence of continence receptors from 1 cm to 3 cm above the anal verge that are responsible for reinforcing the pressure recorded in the proximal anal canal.

We conclude, therefore, that there seem to be mucosal or submucosal receptors in the distal anal canal (at 1 cm to 3 cm from the anal verge) that support the contraction of the external sphincter.

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Practical Consequences of Our Theory of Fecal Continence

An immediate practical consequence of our theory of fecal continence is to avoid resection of the submucosa of the distal 3 cm of the anal canal. Mucosectomy of the distal 3 cm of the anal canal will destroy the AESCR, with serious consequences for fecal continence.

During most of our waking hours and during the entire period of sleep, continence depends on the AESCR. Normally, during wakefulness, we do not need to think about our fecal continence because the AESCR is active during a substantial part of the day. Only after reaching urge sensation are we aware that we need to go to the toilet. Also, during sleep, our fecal continence is taken care of by the anal continence reflex.

If the AESCR is destroyed during perineal or anal surgery or because of trauma, this reflex can no longer support fecal continence. Patients, who are aware of the risk of losing stool during wakefulness, can train themselves to respond to any rectal filling sensation by immediately going to the toilet, thus preserving their fecal continence. During sleep, however, this continence rescue system is inactive, and people with a nonfunctioning AESCR will experience fecal incontinence. This may explain why these patients are fully continent during wakefulness, by evacuation of stools before reaching urge sensation, but incontinent during sleep. The reason is that, during sleep, the mechanism to produce stool before reaching urge sensation is inactive.

Support for our theory comes from the observations reported by others. The incidence of incontinence during sleep is higher after IPAA with mucosectomy than after double-stapled IPAA, 64% and 38%. This is the case despite similar preservation of continence during wakefulness (77% after IPAA with mucosectomy versus 84% after double-stapled IPAA).22 Other researchers also reported a higher incidence of nocturnal soiling in comparison with daytime incontinence after IPAA with mucosectomy, 57% and 4%.23 During wakefulness, continence can be more easily maintained by that part of the external sphincter that is consciously controlled than is the case during sleep.

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CONCLUSION

Our results support the theory that fecal continence by contraction of the external sphincter depends on a spinal reflex, the anal external sphincter continence reflex, without involving the brain. The afferent receptors of this reflex are located in the distal anal canal. Presumably, these are contact receptors that are superficially located in the mucosal or submucosal space. The consequence of this mechanism is that nonfunctioning of the continence reflex possibly results in fecal incontinence.

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ACKNOWLEDGMENTs

The authors thank A. Vandenbosch and O. J. Pras for their substantial assistance in the manometry laboratory, and Prof E. Heineman and Dr T. van Wulfften Palthe for correcting the English manuscript.

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