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106 Colorectal Motility Induction by Sacral Nerve Electrostimulation in a Canine Model [2003년 6월 DCR] 2011-11-17 3477
 
Implications for Colonic Pacing
 
Takeshi Hirabayashi, M.D.,* Hiroshi Matsufuji, M.D.,† Jotaro Yokoyama, M.D.,*Kazuhiko Hagane, M.D.,‡ Ken Hoshino, M.D.,* Yasuhide Morikawa, M.D.,* Masaki Kitajima, M.D.*
 
From the *Department of Surgery, Keio University, Tokyo, Japan, †Pediatric Surgery, St. Luke’s International Hospital, Tokyo, Japan, and ‡Pediatric Surgery, National Tochigi Hospital, Tochigi, Japan
 
PURPOSE: This study investigated the role of the sacral nerves in the mechanism of defecation using adult mongrel dogs. The possibility of designing a colonic pacemaker as a new therapeutic device to treat defecation disturbances, such as fecal incontinence and severe constipation, is also discussed.
METHODS: Colorectal motility during spontaneous defecation was monitored with force strain-gauge transducers implanted in the proximal, distal, and sigmoid colon, rectum, and internal anal sphincter. Under general anesthesia, the sacral nerve was stimulated electrically, and the colorectal motility response was examined.
RESULTS: During spontaneous defecation, three characteristic motility patterns were observed: 1) giant migrating contractions of the colon were propagated to the rectum or anus; 2) the rectum relaxed before the giant migrating contractions were propagated; and 3) the internal anal sphincter was relaxed during the propagation of the giant migrating contraction. Sacral nerve stimulation elicited the following three unique responses: 1) contractile movements were propagated from the distal colon to the rectum; 2) a relaxation response was noted in the rectum; and 3) the internal anal sphincter exhibited a relaxation response. The duration and propagation velocity of the contractile responses and the duration of relaxation responses elicited by electrical stimulation of the sacral nerve were similar to those that
occurred during spontaneous defecation, but their amplitudes were smaller.
CONCLUSION: The coordinated processes of the colon and anorectum during defecation were affected by the sacral nerves. This suggests that it is possible to design a colonic pacemaker to control lower colonic and rectal movements.
 

Since the nineteenth century, it has been reported that intestinal motility is closely related to the central nervous system. For higher forms of life, it is extremely important for their survival and social acceptability that they are able to defecate at the appropriate time and place.
 
Early in the twentieth century, Cannon and Holtzknecht made radiographic observations and described mass movements of the colonic contents toward the anus. These studies were followed by
scintigraphic investigations, which elucidated excretion not only of the rectal contents but also of
the colonic contents during defecation These findings indicated that defecation is not a phenomenon
limited to the rectum and anus but is a synchronized movement involving the colon, rectum, and
anal canal
.
 
Meanwhile, Langley and Anderson conducted detailed pioneering studies on colonic control from the sacral and pelvic nerves, which provided anatomic proof that the right colon is under the control of the vagal parasympathetic nervous system and the sacral parasympathetic nervous system is distributed
in the left colon. The functional importance of the sacral nervous system in defecation has also been recognized. It has been demonstrated clinically that those patients with damage to the sacral nerve, such as spinal cord injuries, sacral anomalies, and myelomeningocele involving the spinal cord, also have defecation disturbances. The canine colon closely anatomically resembles that of humans. Canine food habits and social activities, as well as fecal properties, are also comparable to ours. Therefore, adult mongrel dogs were used in the present study.
 
DISCUSSION
Colonic and rectoanal movements at defecation have been studied separately. This is the first experiment to observe the response of the colon and anorectum to sacral nerve electric stimulation. Observations of colonic movements in dogs by use of a straingauge transducer indicated large contractile waves that originated at the colon and propagated toward the anus at defecation. These were called giant migrating contractions. Similar peristaltic waves, high-amplitude propagating contractions, have been noted in pressure studies in the human colon. Gower was the first to report the inhibitory response of the internal anal sphincter that was elicited by the rectum, which was later named the rectoanal inhibitory reflex by DeGroat and Krier. Observations in the present study indicated that during spontaneous defecation, a series of movement patterns developed through cooperative motility of the colon, rectum, and internal anal sphincter. Such an organized gastrointestinal movement, like the migrating motor complex of the small intestine, is programmed by the enteric nervous system. However, this system is not completely independent; it controls smooth muscle activity while under the control of the central nervous system via efferent and afferent nerves, such as the sympathetic, parasympathetic, and sensory nervous systems.
 
Studies on humans, dogs, and rats have indicated that the distal colon, rectum, and internal anal sphincter are abundantly innervated by extrinsic nerves from the sacral and pelvic nervous systems. Fukai and Fukuda proved anatomically and physiologically the presence of a sacral nerve in the dog that enters the rectum through the pelvic plexus and ascends orally along the colonic wall. It is also known that the internal anal sphincter relaxes when the sacral nerves are stimulated electrically, and it is generally accepted that part of these sacral nerves descends from the rectum to the internal anal sphincter. Studies on acute nerve stimulation and chronic neurectomy experiments proved that the sacral parasympathetic nervous system participates in colonic movements. In the present experiment, responses resembling the motility patterns of the colon, rectum, and internal anal sphincter at spontaneous defecation were reproduced by stimulation of the sacral nerves. These findings suggested the possibility that the defecation movement program under the control of the colonic enteric nervous system is activated through the sacral nerves. The duration of the second GMC during spontaneous
defecation was smaller and the propagation velocity was faster than that of the first GMC. Although
the duration of both contraction and relaxation induced by nervous stimulation resembled that
associated with spontaneous defecation, the amplitudes were smaller. These findings suggest that the
anesthesia at stimulation and the amount of the enteric contents had some influence on these values.
The slow relaxation observed during spontaneous defecation is absent in the response elicited by nervous stimulation, and it is thought to be a receptive relaxation.
 
It was recently proved on the basis of anatomic studies that Barrington’s nucleus, which acts as a
bridge between the central nervous system and the spinal nerves, controls the urination apparatus. It also controls the lower colon via the sacral parasympathetic nervous system. In particular, it is believed
that the nucleus acts as a center to synchronize the functions of the forebrain and sacral parasympathetic nervous system. It was concluded from the present study that the sacral parasympathetic nervous system constitutes an important circuit that connects the central and colonic enteric nervous systems.
 
The Brindley stimulator, which applies electric stimuli to the sacral nerves, has been used to treat
urination disorders in patients with spinal cord injuries. It was reported recently that this device is also effective in ameliorating defecation disorders of spinal cord–damaged patients, although it is associated
with some adverse effects, such as autonomic dysreflexia, spasticity, and sacral segment pain. The intradural nerve stimulation conducted in the present study simultaneously stimulates the pudendal
nerve and causes contraction of the external anal sphincter and other pelvic muscles. For effective stimulation to elicit defecation responses, it is necessary to stimulate the sacral parasympathetic nerves at the periphery of the sacral plexus (Fig. 3).
 

In the present study, an acute experiment was conducted in which electric stimulation was applied directly to the sacral nerves, instead of implanting a stimulator, as would be done in clinical practice. Despite this difference, actual defecatory responses occurred in several animals, which strongly suggests that it may be feasible to design a defecatory pacemaker.