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Colonic dysfunction in patients with thoracic spinal cord injury
(;ASTKOEN7‘E:KoI.o(;Y
1984:86:287-94
Colonic Dysfunction in Patients With Thoracic Spinal Cord Injury MICHAEL E. GLICK, HOOSHANG MESHKINPOUR, SCOTT HALDEMAN, FRED HOEHLER, NANCY DOWNEY, and WILLIAM
E. BRADLEY
IIepartments of Medicine (California and LJniversity
and Neurology, Veterans Administration of California, Irvine, California
Severe constipation is a debilitating concomitant of complete traumatic thoracic spinal cord injury. In order to investigate the pathophysiology of this symptom, we studied colonic compliance, as well as motor and myoelectrical activity, in the fasting and postprandial states and affer neostigmine stimulation in 9 patients with clinically and electrophysiologically documented complete thoracic spinal cord injury. Electrophysiologic studies, including nerve conduction velocities, cortical and spinal somatosensory-evoked responses, and bulbocavernosus reflex responses, as well as urinary bladder cystometry, documented normal peripheral somatosensory function, integrity of the distal spinal cord, conus medullaris and cauda equina, and interruption of the somatosensory and descending spinal pathways proximal to the cauda equina. These 9 patients with spinal cord injury demonstrated a decrease in colonic compliance compared with a control group [p < 0.01). They failed to demonstmte the postprandial increase in colonic motor und myoelectrical activity observed in a control group (p < O.OI), but did respond to neostigmine with an increase in both motor and rnyoelectrical activity (p < 0.02), suggesting an intact myogenic component. In these patients, decreased colonic compliance and absent postprandial colonic motor and myoelectrical activit), may be mediated bjr ablation of outflow from higher centers to the lower spinal cord and may be correlates of visc,eraJ neuropathy and severe constipation. Keceived April 28. 1983. Accepted August 17, 1983. Address requests tar reprints to: Michael E. Glick, M.D.. Veterans Administration Medical Center, 5901 East Seventh Street. Long Beach, California 90822. The authors thank the staff of the Spinal Cord Service at the Long Beach Veterans Administration Medical Center for referring patients for study, Bonnie Johnson and Marcella Palzer for techncal assistance, and Ncadra Leake for preparation of the manuscript. (’ 1984 ~JY the American Gastroenterological Association 001 ii-5l)t)R,'84:$3.00
Medical
Center,
Long Beach.
Complete traumatic thoracic spinal cord injury is associated with urinary bladder dysfunction and intractable constipation. After thoracic spinal cord injury, the urinary bladder empties by automatic reflex contractions upon detrusor distention (l-5). This urinary bladder dysfunction is the cause of significant morbidity and mortality in this population. Severe constipation, requiring daily manual disimpaction, is also a cause of substantial morbidity. Previous studies have demonstrated both abnormal colonic motor activity (6) and compliance (7) in these patients. In order to further investigate the pathophysiology of this intractable constipation, we have studied colonic motor and myoelectrical activity, as well as colonic compliance. in a group of patients with thoracic spinal cord injury and extensive evidence of interruption of the somatosensory and visceral neural pathways central to the lumbar spinal cord.
Subjects Patients
and Methods and
Subjects
Nine patients with a clinical transverse myelytic syndrome were studied. All were men between 22 and 58 yr of age, and all had sustained a traumatic spinal cord injury between 3 mo and 20 yr before investigation. All had anhydrosis and motor and sensory deficits in a distribution consistent with complete spinal cord injury within one dermatome of their vertebral spine injury. All of the patients had symptoms of bladder and bowel dysfunction, including automatic detrusor contractions, urinary incontinence, and severe constipation, requiring bladder catheterization and daily manual disimpaction. All were unable to defecate spontaneously. For each study, normal values were obtained by studying at least 10 volunteers who were asymptomatic for neurologic, urologic, and gastrointestinal disease. These studies were approved by the Human Studies Committee of the Long Beach Veterans Administration Medical Center. October 1981.
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Methods The following studies were performed on each or control subject. Motor and sensory nerve conduction velocity studies. Peripheral motor nerve conduction was studied in the posterior tibia1 nerve by recording potentials in the abductor hallucis muscle on stimulation of the posterior tibia1 nerve at the ankle and at the popliteal fossa (8). Conduction velocity and distal latency values were calculated. Peripheral sensory nerve conduction was studied in an orthodromic fashion by stimulation of the sural nerve at the ahkle and recording over the midcalf. The distal latency, amplitude, and conduction velocity was assessed by computer averaging of 16 responses. Bulbocavernosus reflex responses. Bulbocavernosus reflex responses were studied by stimulating the dorsal nerve of the penis with ring electrodes while recording potentials in the pelvic floor muscles with a surface electrode placed in the midperineum and a reference electrode placed over the iliac crest (9). The latency of the response was assessed by computer averaging of 100 responses. Each study was performed three times to ensure reproducibility. Somatosensory-evoked potentials. Somatosensory-evoked potentials were recorded on stimulation of the posterior tibia1 nerve at the ankle (10). Spinal cord potentials were recorded by means of surface electrodes placed at the L-l level with the reference electrode at the L-5 spinous process. Cortical potentials were recorded over the scalp in the midline, 2 cm behind the Cz electroencephalographic recording site, and referenced to the forehead. The averaged response to 1000 stimuli was recorded, and each study was performed three times to ensure reproducibility. In a similar fashion, somatosensory responses were recorded on stimulation of the pudendal nerve (9). Cystometrogram. Cystometry was performed by introducing carbon dioxide into the bladder through a transurethral catheter at a rate of 150 mlimin while recording intravesicular pressure. The onset of detrusor contraction, as marked by a rapid rise in intravesicular pressure, was determined. The ability of the patients to voluntarily suppress the detrusor contraction was assessed (11). Colopic compliance. All medications known to effect gastrointestinal function were withheld for at least 24 h before study. After an overnight fast, a noncompliant catheter was placed in the rectum and perfused by a low compliance pneumohydraulic pump (Arndorfet Medical Specialties, Greendale, Wise.). The catheter was connected to a volume displacement transducer (Statham P-518, Gould, Inc., Cleveland, Ohio) and a dynograph recorder (Beckman R-612, Beckman Instruments, Inc., Fullerton, Calif.). Tap water was allowed to drain into the rectum at the rate of 100 mlimin while intracolonic pressure was monitored continuously. All studies were performed with the subjects in the left lateral decubitus position. Each recording was continued until either a maximum of 2400 ml of tap water was instilled or a maximum intracolonic pressure of 40 mmHg was recorded. Colonic motor and myoelectrical activity. Colonic patient
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motor and myoelectrical activity were recorded as previously described (12). After an overnight fast, a bipolar suction electrode assembly (13) was introduced through a sigmoidoscope and was anchored to the mucosa 12-18 cm from the anal verge by applying lo-15 mmHg of negative pressure. Patients did not receive enemas or air insufflation before or during the sigmoidoscopy. The bipolar electrode was connected to a patient isolator with a maximum rating of 10 I_LAt 200 V (Model IS-3dp, OHMIC Instruments, St. Michaels, Md.). The isolator was in turn connected to a coupler with a time constant of 1.0 s (0.16 Hz) and a 25-Hz low pass filter (Beckman Model 9859). Colonic intraluminal pressure was recorded using a polyvinyl catheter with an internal diameter of 1.1 mm, a low compliance pneumohydraulic pump (Arndorfer Medical and a volume displacement transducer Specialties), (Statham P-518). The pressure-measuring assembly was calibrated in millimeters of mercury using a mercury-filled sphygmomanometer. Respirations were monitored with a pneumograph belt placed around the chest. Myoelectrical signals, intraluminal pressure, and pneumogram were monitored on a rectilinear recorder (Beckman R-612) and were simultaneously recorded on a J-channel FM tape recorder (Model C-4, A.R. Vetter, Rebersburg, Pa.]. In addition, myoelectrical signals were filtered through a variable band pass filter (KH-3700, Krohn-Hite Corp., Avon, Mass.) that allowed only transmission of signals with a frequency between 8.0 Hz and 13.0 Hz. The band pass filter removed all slow wave activity and allowed only spike activity to be recorded. Spike potentials appeared as rapid fluctuations of electrical potentials that were not associated with simultaneous movement artifact on respiration or pressure recordings. Because of difficulty in accurately determining the number of individual spikes present in a burst, only one spike potential was counted per slow wave cycle. Only spike potentials >0.02 mV were counted. The motor activity of the rectosigmoid area was quantified by a Tetronix 4051 computer (Tetronix Corporation, Portland, Ore.] that digitized the voltage output of the recorder at a rate of 100 Hz and determined the mean amplitude of the signals over 15-min intervals. The lowest artifact-free pressure measurement for each 15-min interval was selected as a baseline. The motor activity is expressed as mean amplitude in millimeters of mercury for each 15-min interval. After a 30-min adaptation period (13), a baseline mean amplitude motor activity was determined over 15 min. Each subject then received a lOOO-kcal meal consisting of a roast beef sandwich with mayonnaise and 240 ml of vanilla milk shake. The nutritional content of the meal, estimated from the food portions, was 45% fat, 20% protein, and 35% carbohydrate (14). Each patient ingested the meal within 7-10 min. Recording continued for 90 min after the meal was served. After the 90-min postprandial recording period, 1 mg of neostigmine was administered subcutaneously. Recordings continued for an additional 45 min or until patients experienced diaphoresis or abdominal cramping. These symptoms were treated with a subcutaneous injection of atropine. Statistical analysis was made both with paired and unpaired Student’s t-tests as well as with the MannWhitney test. All values are expressed as mean i- SEM.
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1984
h
Spinal
Cord Injury n=?
8
10
VOLUME Figure
I. Colonic
compliance injury is compared infusion increment
(100
14
16
18
20
22
24
ml water)
curves. A composite of the colonic compliance curves from 7 patients with complete thoracic spinal cord with a composite from 10 controls. The mean intracolonic pressure recorded at each 100 ml of water in the spinal cord injury group was greater than that recorded in the control group (p < 0.01).
Results Nerve Conduction
Motor and Sensory Velocities Motor and sensory ties were obtained from the patients with spinal cord normal motor and sensory ties, amplitudes, and distal normal motor and sensory tem function in the lower
Bulbocavernosus Bulbocavernosus elicited in all 9 patients demonstrated normal reflex response tests the cord, conus medullaris,
12
nerve conduction velocilower extremities in all 9 injury. All patients had nerve conduction velocilatencies, demonstrating peripheral nervous sysextremities (8).
Reflex
Responses
reflex responses were easily with spinal cord injury and latencies (28-46 ms). This integrity of the distal spinal and cauda equina (15-17).
Somatosensory-Evoked
ducibly elicited. Of the 9 patients with spinal cord injury, 6 had normal spinal-evoked responses on stimulatioi of the posterior tibia1 nerve, demonstrating normal somatosensory nerve conduction from the posterior tibia1 stimulation site to the recording site at the L-lregion of the spinal cord. In 3 patients with spinal cord injury, posterior tibia1 somatosensory-evoked responses could not be detected. However, absence of a recordable spinal response. may have been due to obesity or to difficulty with anatomic placement of‘ the recording electrodes (9). All 9 patients with spinal cord injury had absent cortical somatosensory-evoked responses upon stimulation of the posterior tibia1 nerve. The absence of cortical somatosensory-evoked responses in the patients with normal spinal-evoked responses on stimulation of the posterior tibia1 nerve demonstrated interruption of transmission in the somatosensory axis between the L-l region of the cord, where the signal was normal, and the cortex, where the signal did not appear (10,18,19).
Potentials
In normal volunteers, spinaland corticalevoked potentials upon stimulation of the posterior tibia1 and pudendal nerves can be easily and repro-
Cystometrogram In all 9 patients with spinal cord cystometrogram was markedly abnormal.
injury, the Seven of
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GASTROENTEROLOGY
ET AL.
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0
Control8(n -11
m
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f
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12
5
4
0
Baseline
#
o-15
15-30
30-45
45-60
60-75
75-90
Meal TIME Figure
PERIOD
2. Mean amplitude of the colonic motor activity from 9 patients 11 cUntro1 subjects. Although normal volunteers demonstrated the patients with spinal cord injury had no response
these patients had a hyperreflexic cystometrogram, with a marked increase in intravesicular pressure at volumes ~150 ml CO*, and were unable to inhibit the detrusor reflex. The other 2 patients demonstrated an areflexic cystometrogram, which may also be the sequela of thoracic spinal cord injury (2,ll). This detrusor areflexia has been attributed to damaged innervation of the detrusor muscle from recurrent bladder infections and overdistention (11,201, which may be related to bladder neck obstruction from detrusor hypertrophy or cystosphincteric dyssynergia (4,5). Colonic Compliance Seven of the patients with spinal cord injury demonstrated an abnormal colonic compliance. In these patients, a rapid pressure rise was observed upon instillation of a small volume of water. In 2 patients, an adequate seal between an occluding balloon and the rectum could not be maintained and colonic volume-pressure curves could not be recorded. In Figure 1, composite tracings of colonic compliance curves from 10 normal volunteers and from the 7 patients with spinal cord injury are demonstrated. In each patient with spinal cord injury
(mlnuted
with thoracic spinal cord injury is compared with the results from a postprandial increase in motor activity (p < 0.01 vs. baseline),
studied, the intracolonic pressure exceeded 40 mmHg, with an infusion volume between 400 and 600 ml of water. The mean intracolonic pressure recorded at each 100 ml of water infusion increment in the spinal cord injury group was greater than that recorded in the control group (p < 0.01). The infusion volume necessary to reach an intracolonic pressure of 40 mmHg in the spinal cord injury group was -25% of the volume required in the control group. Colonic Motor and Myoelectrical
Activity
The mean amplitude of the colonic motor activity for each 15min period from 11 control subjects and from the 9 patients with spinal cord injury is shown in Figure 2. In the normal volunteers, there was an increase in the motor activity in the first 15-min interval after the meal (p < 0.01). This increase in motor activity persisted through the second postprandial 15-min interval (p < 0.01). The motor activity returned to the preprandial state during the third 15-min period after the meal. In the patients with spinal cord injury, the baseline mean amplitude motor activity was similar to that seen in the control group. However, there was no significant increase in the motor activity after the meal.
Februarp
COLONIC
1984
Baseline
f
O-15
15-30
30-45
DYSFUNCTION
0
Controls
m
Spinal
SC1
291
h=ll)
Cord
45-60
IS THORACIC
Injury
60-75
(n=9)
75-90
Meal TIME PERIOD Figure
(minutes)
3. Colonic myoelectrical spike potential frequency from 9 patients with thoracic spinal cord injury is compared from 11 control subjects. Although normal volunteers demonstrated a postprandial increase in myoelectrical frequency (p < 0.01 vs. baseline], the patients with spinal cord injury had no response.
The colonic myoelectrical spike potential frequencies recorded in the normal controls and in the patients with spinal cord injury are shown in Figure 3. Coincident with the increase in the mean amplitude of colonic motor activity, normal control subjects demonstrated an increase in the number of spike potentials in the first 15-min interval after the meal (p < 0.02). This increase persisted through the second postprandial 15-min interval (p < 0.01). The frequency of spike potentials returned toward their preprandial levels during the third and fourth l5min postprandial periods. However, in the patients with spinal cord injury, the frequency of spike potentials did not change after the meal.
Colonic Motor and Myoelectrical Activity Response to Neostigmine Stimulation The colonic motor and myoelectrical response to the subcutaneous administration of 1 mg of neostigmine in the 6 patients with spinal cord injury studied is demonstrated in Figures 4 and 5. The patients with spinal cord injury responded to neostigmine stimulation with an increase in both motor and myoelectrical activity (p < 0.02).
with the results spike potential
Discussion The electrodiagnostic assessment of motor and sensory nerve conduction velocities is a sensitive method for the evaluation of peripheral nerve function. All of the patients with thoracic spinal cord injury demonstrated normal peripheral nerve conduction. Somatosensory-evoked responses evaluate sensory conduction in the dorsal column of the spinal cord (10,18,19). The spinal-evoked response. on stimulation of the posterior tibia1 nerve, measures the peripheral conduction time in afferent somatic: nerves between the stimulation and the recording sites. The cortical response measures the conduction time in peripheral afferent somatic nerves plus the central conduction time through the dorsal column and brain stem pathways to the sensory cortex (10,18,19). Absent cortical somatosensory-evoked responses upon stimulation of the posterior tibia1 nerve in the presence of normal spinal somatosensory-evoked responses, as seen in most of our patients with spinal cord injury, suggests a lesion within the spinal cord dorsal column pathways. The bulbocavernosus reflex response tests a reflex loop that includes both sensory and motor pudendal fibers
292
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Bas:line THORACIC
Figure
SPINAL
CORD
Post Neostigmine INJURY
PATIENTS
4. The colonic motor activity in response to parenteral injection of 1 mg of neostigmine is compared with the baseline activity in 6 patients with thoracic spinal cord injury. The patients responded to neostigmine stimulation with an increase in motor activity (p < 0.02).
and conduction through the sacral spinal cord (l517). A normal bulbocavernosus reflex response suggests integrity of the distal spinal cord, conus medullaris, and cauda equina. The measurement of spinal, cortical, and bulbocavernosus responses on stimulation of the pudendal nerve permits the evaluation of conduction in peripheral afferent, central, conus medullaris, and peripheral efferent components of this nerve. These studies demonstrate the integrity of these somatic pathways below the level of L-l, and the disruption central to L-l. Detrusor hyperreflexia is the most common cystometric disturbance described in spinal cord injury (l-5). The contraction of the urinary bladder in response to distention is mediated by a spinal reflex mechanism. In normal individuals, this reflex is inhibited by input from higher centers in the brain (21,22). The interruption of descending spinal pathways causes contractions of the bladder in the presence of smaller-than-normal degrees of organ distention and prevents voluntary suppression of these contractions (23). In our patients with spinal cord injury, the abnormal cortical somatosensory-evoked response studies and the abnormal cystometrogranrs suggest interruption of both ascending somatosensory and descending visceral pathways between the lumbar spinal cord and the cortex. The study of volume-pressure curves of the colon,
Vol. 86, No. 2
for the characterization of neurologic disturbances, was first described in 1940 (24). These studies suggested that lesions of the motor fibers in the brain or descending spinal tracts were associated with “hyper-reflexic” or rapid-rise volume-pressure curves, whereas lesions in the sacral segments of the cauda equina or pelvic plexus caused an “areflexic” or flat volume-pressure curve. Studies in the cat (25) confirmed these observations. A recent report (7) confirmed this decrease in colonic compliance in patients with evidence of traumatic transverse thoracic spinal cord injury on clinical examination. Our patients, selected for their extensive electrodiagnostic and clinical evidence of complete thoracic spinal cord injury, confirmed these findings. The increased slope of the colonic volume pressure curves in our patients was analagous to the hyperreflexic cystosuggesting the same neuropathometrograms, physiology. To assess colonic motor activity in these patients, motor and myoelectrical activities were recorded in a resting state and after ingestion of a meal. The baseline mean amplitude of colonic motor activity in the patients with spinal cord injury was similar to that observed in the control population. However, the patients with spinal cord injury failed to demonstrate the postprandial increase in colonic motility
9-
a7
-’
6-
5-
4-
3-
2-
l-
Post
Baseline
Neostigmine THORACIC
SPINAL
CORD
INJURY
PATIENTS
The colonic myoelectrical activity in response to parenteral injection of 1 mg of neostigmine is compared with the baseline activity in 6 patients with thoracic spinal cord injury. The patients responded to neostigmine stimulation with an increase in myoelectrical activity (p i 0.02).
February
1984
observed in the control population. Spike potentials represent the electrical manifestations of smooth muscle contraction, and, hence, the myoelectrical spike potential frequency can be expected to parallel the motor activity. The baseline spike potential frequency observed in the patients with spinal cord injury was similar to that observed in the control population. However, unlike the control population, these patients with spinal cord injury failed to demonstrate a postprandial increase in spike potential frequency. Thus, these myoelectrical recordings confirmed the measurements of colonic motor activity. The motility of the pelvic colon in patients with a clinical examination compatible with injury to the thoracic spinal cord has been reported to demonstrate increased baseline activity (6). There are several explanations for the discrepancy between this previous study and our current observations. The group of patients reported by Connell (6) was a poorly defined and heterogeneous population, including patients with spinal cord injury from a variety of lesions, such as trauma, tumors, and alcohol injections. Some patients had spastic and some flaccid paralysis, and all were defined solely by physical examination rather than by electrodiagnosis. In addition, in the study reported by Connell, a different recording technique was used. Connell reported a postprandial increase in colonic motor activity in his patients with thoracic spinal cord injury. However, other studies suggest that the nervous system must be intact to mediate the postprandial colonic motor and myoelectrical response (12,26). In patients with advanced multiple sclerosis and extensive clinical and electrodiagnostic evidence of interruption of the spinal cord, the postprandial colonic response was absent (12). Lastly, the absence of the postprandial motor and myoelectrical response in diabetic patients with autonomic neuropathy and severe constipation (26) suggests that this response can be blocked by peripheral, as well as by central, nervous system dysfunction. Although several studies have suggested hormonal mediation of the postprandial colonic motor and myoelectrical response (27-29), the absent response in patients with peripheral and central nervous system dysfunction suggests that, if there is a hormonal component to this response, this hormonal component is integrated by the nervous system. Impaired gastroduodenal function cannot be implicated in the absent postprandial colonic motor and myoelectrical response in patients with diabetes mellitus or thoracic spinal cord injury. Diabetic patients with autonomic neuropathy who lacked the postprandial colonic response had normal gastric emptying (26). In addition, patients with complete thoracic spinal cord injury had normal gastric emp-
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tying and normal interdigestive antral-duodenal motor coordination (30). To exclude a myogenic component to the impaired postprandial colonic motor and myoelectrical response, we studied the colonic response to neostigmine stimulation (28,31). The increase in motor and myoelectrical activity in response to neostigmine stimulation demonstrated by our patients provides evidence for an intact myogenic component, suggesting that the absent response is neurogenic in origin. Patients with extensive clinical and electrodiagnostic evidence of somatosensory and visceral complete transverse thoracic spinal cord injury have abnormal colonic compliance and absent postprandial colonic motor and myoelectrical responses. However, these patients respond to neostigmine stimulation with a normal increase in colonic motor and myoelectrical activity, suggesting an intact myogenie component. These data suggest that the central nervous system is essential for the mediation of the postprandial colonic increase in motor and myoelectrical activity. In patients with thoracic spinal cord injury, abnormal colonic compliance and absent postprandial colonic motor and myoelectrical responses may be mediated by ablation of outflow from higher centers to the lower spinal cord and may be correlates of visceral neuropathy and severe constipation.
References 1. Bors E. Neurogenic bladder. Ural Surv 1957;7:177-250. 2. Rossier A, Bors E. Detrusor responses to perineal and rectal stimulation in patients with spinal cord injuries. Ural Int 1964;18:181-90. 3. Rossier AB, Ott R. Urinary manometry in spinal cord injury. Br J Uro1 1974;46:439-48. 4. Yalla SV, Rossier AB, Fam B. Synchronous cystosphincterometry in patients with spinal cord injury. Urology 1975: 6:777-a. 5. Yalla SV, Rossier AB, Fam B. Dyssynergic vesicourethral responses during bladder rehabilitation in spinal cord injury patients: effects of suprapubic percussion, crede method and bethanechol chloride. J Urol 1976;115:575-9. 6. Connell AM, Frankel H, Guttmenn L. The motility of the pelvic colon following complete lesions of the spinal cord. Paraplegia 1963;1:98-115. 7. Meshkinpour H, Nowroozi F, Glick ME. Colonic compliance in patients with spinal cord injury. Arch Phys Med Rehabil 1983;64:111-2. J, Eberstein A. Electrodiagnosis of neuromuscular 8. Goodgold disease. Baltimore, Md.: Williams & Wilkins, 1972. S, Bradley WE, Bhatia NN, Johnson BK. Pudendal 9. Haldeman evoked responses. Arch Neurol 1982;39:280-3. 10. Jones SJ, Small DG. Spinal and sub-cortical evoked potentials following stimulation of the posterior tibia1 nerve in man. Electroencephalogr Clin Neurophysiol 1978:44:299-306. 11. Raz S, Bradley WE. Neuromuscular dysfunction of the lower urinary tract. In: Harrison JH. Gilles RF, Perlmutter AD, et al..
294
12.
13.
14. 15.
16.
GLICK
ET AL.
eds. Cambell’s urology. Philadelphia: WB Saunders, 1979: 1215-72. Glick ME, Meshkinpour H, Haldeman S, Bhatia NN, Bradley WE. Colonic dysfunction in multiple sclerosis. Gastroenterology 1982;83:1002-7. Taylor I, Duthie HL, Smallwood R, et al. The effect of stimulation on the myoelectrical activity of the rectosigmoid in man. Gut 1974;15:599-607. Bowes A. Bowes and Church’s food values of portions commonly used. 13th ed. New York: Harper & Row, 1980. Ertekin C, Reel F. Bulbocavernosus reflex in normal men and in patients with neurogenic bladder and/or impotence. J Neurol Sci 1976;28:1-15. Dick HC, Bradley WE, Scott FB, Timm GW. Pudendal sexual reflexes: electrophysiologic investigations. Urology 1974; 3:376-g.
17. Siroky MB, Sax DS, Krane RJ. Sacral signal tracing: the electrophysiology of the bulbocavernosus reflex. J Ural 1979; 122:661-4. 18. Eisen A, Elleker G. Sensory nerve stimulation and evoked cerebral potentials. Neurology 1980;30:1097-105, 19. Cusick JF, Myklebest JB, Larson SJ, Sances A. Spinal cord evaluation by cortical evoked responses. Arch Nemo1 1979; 36:140-3. 20. Bradley WE, Chou S, Markland C. Classifying neurologic dysfunction in the urinary bladder. In: Boyarsky S, ed. The neurogenic bladder. Baltimore, Md.: Williams & Wilkins. 1967: 139-46. 21. Kuru M. Nervous control of micturition. Physiol Rev 1965: 45:425-94.
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22. Barrington FJF. The relation of the hind-brain to micturition. Brain 1921;44:23. 23. Bradley WE, Timm GW. Scott FB. Cystometry II: central nervous system organization of detrusor reflex. CJrology 1975; 5~578-80. 24. White JC, Verlot MC, Ehrentheil 0. Neurogenic disturbances of the colon and their investigation by the colonometrogram. Ann Surg 1940;112:1042-57. 25. Scott HW, Cantrell JR. Colonometrographic studies of the effects of section of the parasympathetic nerves of the colon. Bull Johns Hopkins Hosp 1949;85:310-9. 26. Battle WM, Snape WJ, Alavi A, et al. Colonic dysfunction in diabetes mellitus. Gastroenterology 1980;79:1217-21. 27. Snape WJ, Matarazoo SA, Cohen S. Effect of eating and gastrointestinal hormones on human colonic myoelectrical and motor activity. Gastroenterology 1978;75:373-8. 28. Snape WJ, Carlson GM. Cohen S. Human colonic myoelectrical activity in response to prostigmin and the gastrointestinal hormones. Am J Dig Dis 1977:22:881-8. 29. Dinoso VP, Meshkinpour H, Lorber SH. et al. Motor responses of the sigmoid colon and rectum to exogenous cholecystokinin and secretion. Gastroenterology 1973;65:438-44. 30. Fealey RD, Szurszewski JH, Merritt JL, DiMagno EP. The effect of traumatic spinal cord transection on human upper gastrointestinal motility (abstr). Gastroenterology 1982; 82:1053. 31. Chaudhary NA. Truelove SC. Human colonic motility: a comparative study of normal subjects, patients with ulcerative colitis, and patients with the irritable colon syndrome. II. The effect of prostigmin. Gastroenterology 1961;40:18-26.
1984:86:287-94
Colonic Dysfunction in Patients With Thoracic Spinal Cord Injury MICHAEL E. GLICK, HOOSHANG MESHKINPOUR, SCOTT HALDEMAN, FRED HOEHLER, NANCY DOWNEY, and WILLIAM
E. BRADLEY
IIepartments of Medicine (California and LJniversity
and Neurology, Veterans Administration of California, Irvine, California
Severe constipation is a debilitating concomitant of complete traumatic thoracic spinal cord injury. In order to investigate the pathophysiology of this symptom, we studied colonic compliance, as well as motor and myoelectrical activity, in the fasting and postprandial states and affer neostigmine stimulation in 9 patients with clinically and electrophysiologically documented complete thoracic spinal cord injury. Electrophysiologic studies, including nerve conduction velocities, cortical and spinal somatosensory-evoked responses, and bulbocavernosus reflex responses, as well as urinary bladder cystometry, documented normal peripheral somatosensory function, integrity of the distal spinal cord, conus medullaris and cauda equina, and interruption of the somatosensory and descending spinal pathways proximal to the cauda equina. These 9 patients with spinal cord injury demonstrated a decrease in colonic compliance compared with a control group [p < 0.01). They failed to demonstmte the postprandial increase in colonic motor und myoelectrical activity observed in a control group (p < O.OI), but did respond to neostigmine with an increase in both motor and rnyoelectrical activity (p < 0.02), suggesting an intact myogenic component. In these patients, decreased colonic compliance and absent postprandial colonic motor and myoelectrical activit), may be mediated bjr ablation of outflow from higher centers to the lower spinal cord and may be correlates of visc,eraJ neuropathy and severe constipation. Keceived April 28. 1983. Accepted August 17, 1983. Address requests tar reprints to: Michael E. Glick, M.D.. Veterans Administration Medical Center, 5901 East Seventh Street. Long Beach, California 90822. The authors thank the staff of the Spinal Cord Service at the Long Beach Veterans Administration Medical Center for referring patients for study, Bonnie Johnson and Marcella Palzer for techncal assistance, and Ncadra Leake for preparation of the manuscript. (’ 1984 ~JY the American Gastroenterological Association 001 ii-5l)t)R,'84:$3.00
Medical
Center,
Long Beach.
Complete traumatic thoracic spinal cord injury is associated with urinary bladder dysfunction and intractable constipation. After thoracic spinal cord injury, the urinary bladder empties by automatic reflex contractions upon detrusor distention (l-5). This urinary bladder dysfunction is the cause of significant morbidity and mortality in this population. Severe constipation, requiring daily manual disimpaction, is also a cause of substantial morbidity. Previous studies have demonstrated both abnormal colonic motor activity (6) and compliance (7) in these patients. In order to further investigate the pathophysiology of this intractable constipation, we have studied colonic motor and myoelectrical activity, as well as colonic compliance. in a group of patients with thoracic spinal cord injury and extensive evidence of interruption of the somatosensory and visceral neural pathways central to the lumbar spinal cord.
Subjects Patients
and Methods and
Subjects
Nine patients with a clinical transverse myelytic syndrome were studied. All were men between 22 and 58 yr of age, and all had sustained a traumatic spinal cord injury between 3 mo and 20 yr before investigation. All had anhydrosis and motor and sensory deficits in a distribution consistent with complete spinal cord injury within one dermatome of their vertebral spine injury. All of the patients had symptoms of bladder and bowel dysfunction, including automatic detrusor contractions, urinary incontinence, and severe constipation, requiring bladder catheterization and daily manual disimpaction. All were unable to defecate spontaneously. For each study, normal values were obtained by studying at least 10 volunteers who were asymptomatic for neurologic, urologic, and gastrointestinal disease. These studies were approved by the Human Studies Committee of the Long Beach Veterans Administration Medical Center. October 1981.
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Methods The following studies were performed on each or control subject. Motor and sensory nerve conduction velocity studies. Peripheral motor nerve conduction was studied in the posterior tibia1 nerve by recording potentials in the abductor hallucis muscle on stimulation of the posterior tibia1 nerve at the ankle and at the popliteal fossa (8). Conduction velocity and distal latency values were calculated. Peripheral sensory nerve conduction was studied in an orthodromic fashion by stimulation of the sural nerve at the ahkle and recording over the midcalf. The distal latency, amplitude, and conduction velocity was assessed by computer averaging of 16 responses. Bulbocavernosus reflex responses. Bulbocavernosus reflex responses were studied by stimulating the dorsal nerve of the penis with ring electrodes while recording potentials in the pelvic floor muscles with a surface electrode placed in the midperineum and a reference electrode placed over the iliac crest (9). The latency of the response was assessed by computer averaging of 100 responses. Each study was performed three times to ensure reproducibility. Somatosensory-evoked potentials. Somatosensory-evoked potentials were recorded on stimulation of the posterior tibia1 nerve at the ankle (10). Spinal cord potentials were recorded by means of surface electrodes placed at the L-l level with the reference electrode at the L-5 spinous process. Cortical potentials were recorded over the scalp in the midline, 2 cm behind the Cz electroencephalographic recording site, and referenced to the forehead. The averaged response to 1000 stimuli was recorded, and each study was performed three times to ensure reproducibility. In a similar fashion, somatosensory responses were recorded on stimulation of the pudendal nerve (9). Cystometrogram. Cystometry was performed by introducing carbon dioxide into the bladder through a transurethral catheter at a rate of 150 mlimin while recording intravesicular pressure. The onset of detrusor contraction, as marked by a rapid rise in intravesicular pressure, was determined. The ability of the patients to voluntarily suppress the detrusor contraction was assessed (11). Colopic compliance. All medications known to effect gastrointestinal function were withheld for at least 24 h before study. After an overnight fast, a noncompliant catheter was placed in the rectum and perfused by a low compliance pneumohydraulic pump (Arndorfet Medical Specialties, Greendale, Wise.). The catheter was connected to a volume displacement transducer (Statham P-518, Gould, Inc., Cleveland, Ohio) and a dynograph recorder (Beckman R-612, Beckman Instruments, Inc., Fullerton, Calif.). Tap water was allowed to drain into the rectum at the rate of 100 mlimin while intracolonic pressure was monitored continuously. All studies were performed with the subjects in the left lateral decubitus position. Each recording was continued until either a maximum of 2400 ml of tap water was instilled or a maximum intracolonic pressure of 40 mmHg was recorded. Colonic motor and myoelectrical activity. Colonic patient
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motor and myoelectrical activity were recorded as previously described (12). After an overnight fast, a bipolar suction electrode assembly (13) was introduced through a sigmoidoscope and was anchored to the mucosa 12-18 cm from the anal verge by applying lo-15 mmHg of negative pressure. Patients did not receive enemas or air insufflation before or during the sigmoidoscopy. The bipolar electrode was connected to a patient isolator with a maximum rating of 10 I_LAt 200 V (Model IS-3dp, OHMIC Instruments, St. Michaels, Md.). The isolator was in turn connected to a coupler with a time constant of 1.0 s (0.16 Hz) and a 25-Hz low pass filter (Beckman Model 9859). Colonic intraluminal pressure was recorded using a polyvinyl catheter with an internal diameter of 1.1 mm, a low compliance pneumohydraulic pump (Arndorfer Medical and a volume displacement transducer Specialties), (Statham P-518). The pressure-measuring assembly was calibrated in millimeters of mercury using a mercury-filled sphygmomanometer. Respirations were monitored with a pneumograph belt placed around the chest. Myoelectrical signals, intraluminal pressure, and pneumogram were monitored on a rectilinear recorder (Beckman R-612) and were simultaneously recorded on a J-channel FM tape recorder (Model C-4, A.R. Vetter, Rebersburg, Pa.]. In addition, myoelectrical signals were filtered through a variable band pass filter (KH-3700, Krohn-Hite Corp., Avon, Mass.) that allowed only transmission of signals with a frequency between 8.0 Hz and 13.0 Hz. The band pass filter removed all slow wave activity and allowed only spike activity to be recorded. Spike potentials appeared as rapid fluctuations of electrical potentials that were not associated with simultaneous movement artifact on respiration or pressure recordings. Because of difficulty in accurately determining the number of individual spikes present in a burst, only one spike potential was counted per slow wave cycle. Only spike potentials >0.02 mV were counted. The motor activity of the rectosigmoid area was quantified by a Tetronix 4051 computer (Tetronix Corporation, Portland, Ore.] that digitized the voltage output of the recorder at a rate of 100 Hz and determined the mean amplitude of the signals over 15-min intervals. The lowest artifact-free pressure measurement for each 15-min interval was selected as a baseline. The motor activity is expressed as mean amplitude in millimeters of mercury for each 15-min interval. After a 30-min adaptation period (13), a baseline mean amplitude motor activity was determined over 15 min. Each subject then received a lOOO-kcal meal consisting of a roast beef sandwich with mayonnaise and 240 ml of vanilla milk shake. The nutritional content of the meal, estimated from the food portions, was 45% fat, 20% protein, and 35% carbohydrate (14). Each patient ingested the meal within 7-10 min. Recording continued for 90 min after the meal was served. After the 90-min postprandial recording period, 1 mg of neostigmine was administered subcutaneously. Recordings continued for an additional 45 min or until patients experienced diaphoresis or abdominal cramping. These symptoms were treated with a subcutaneous injection of atropine. Statistical analysis was made both with paired and unpaired Student’s t-tests as well as with the MannWhitney test. All values are expressed as mean i- SEM.
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h
Spinal
Cord Injury n=?
8
10
VOLUME Figure
I. Colonic
compliance injury is compared infusion increment
(100
14
16
18
20
22
24
ml water)
curves. A composite of the colonic compliance curves from 7 patients with complete thoracic spinal cord with a composite from 10 controls. The mean intracolonic pressure recorded at each 100 ml of water in the spinal cord injury group was greater than that recorded in the control group (p < 0.01).
Results Nerve Conduction
Motor and Sensory Velocities Motor and sensory ties were obtained from the patients with spinal cord normal motor and sensory ties, amplitudes, and distal normal motor and sensory tem function in the lower
Bulbocavernosus Bulbocavernosus elicited in all 9 patients demonstrated normal reflex response tests the cord, conus medullaris,
12
nerve conduction velocilower extremities in all 9 injury. All patients had nerve conduction velocilatencies, demonstrating peripheral nervous sysextremities (8).
Reflex
Responses
reflex responses were easily with spinal cord injury and latencies (28-46 ms). This integrity of the distal spinal and cauda equina (15-17).
Somatosensory-Evoked
ducibly elicited. Of the 9 patients with spinal cord injury, 6 had normal spinal-evoked responses on stimulatioi of the posterior tibia1 nerve, demonstrating normal somatosensory nerve conduction from the posterior tibia1 stimulation site to the recording site at the L-lregion of the spinal cord. In 3 patients with spinal cord injury, posterior tibia1 somatosensory-evoked responses could not be detected. However, absence of a recordable spinal response. may have been due to obesity or to difficulty with anatomic placement of‘ the recording electrodes (9). All 9 patients with spinal cord injury had absent cortical somatosensory-evoked responses upon stimulation of the posterior tibia1 nerve. The absence of cortical somatosensory-evoked responses in the patients with normal spinal-evoked responses on stimulation of the posterior tibia1 nerve demonstrated interruption of transmission in the somatosensory axis between the L-l region of the cord, where the signal was normal, and the cortex, where the signal did not appear (10,18,19).
Potentials
In normal volunteers, spinaland corticalevoked potentials upon stimulation of the posterior tibia1 and pudendal nerves can be easily and repro-
Cystometrogram In all 9 patients with spinal cord cystometrogram was markedly abnormal.
injury, the Seven of
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0
Control8(n -11
m
SpInal Cord Injury (n-Q)
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2
f
16
12
5
4
0
Baseline
#
o-15
15-30
30-45
45-60
60-75
75-90
Meal TIME Figure
PERIOD
2. Mean amplitude of the colonic motor activity from 9 patients 11 cUntro1 subjects. Although normal volunteers demonstrated the patients with spinal cord injury had no response
these patients had a hyperreflexic cystometrogram, with a marked increase in intravesicular pressure at volumes ~150 ml CO*, and were unable to inhibit the detrusor reflex. The other 2 patients demonstrated an areflexic cystometrogram, which may also be the sequela of thoracic spinal cord injury (2,ll). This detrusor areflexia has been attributed to damaged innervation of the detrusor muscle from recurrent bladder infections and overdistention (11,201, which may be related to bladder neck obstruction from detrusor hypertrophy or cystosphincteric dyssynergia (4,5). Colonic Compliance Seven of the patients with spinal cord injury demonstrated an abnormal colonic compliance. In these patients, a rapid pressure rise was observed upon instillation of a small volume of water. In 2 patients, an adequate seal between an occluding balloon and the rectum could not be maintained and colonic volume-pressure curves could not be recorded. In Figure 1, composite tracings of colonic compliance curves from 10 normal volunteers and from the 7 patients with spinal cord injury are demonstrated. In each patient with spinal cord injury
(mlnuted
with thoracic spinal cord injury is compared with the results from a postprandial increase in motor activity (p < 0.01 vs. baseline),
studied, the intracolonic pressure exceeded 40 mmHg, with an infusion volume between 400 and 600 ml of water. The mean intracolonic pressure recorded at each 100 ml of water infusion increment in the spinal cord injury group was greater than that recorded in the control group (p < 0.01). The infusion volume necessary to reach an intracolonic pressure of 40 mmHg in the spinal cord injury group was -25% of the volume required in the control group. Colonic Motor and Myoelectrical
Activity
The mean amplitude of the colonic motor activity for each 15min period from 11 control subjects and from the 9 patients with spinal cord injury is shown in Figure 2. In the normal volunteers, there was an increase in the motor activity in the first 15-min interval after the meal (p < 0.01). This increase in motor activity persisted through the second postprandial 15-min interval (p < 0.01). The motor activity returned to the preprandial state during the third 15-min period after the meal. In the patients with spinal cord injury, the baseline mean amplitude motor activity was similar to that seen in the control group. However, there was no significant increase in the motor activity after the meal.
Februarp
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1984
Baseline
f
O-15
15-30
30-45
DYSFUNCTION
0
Controls
m
Spinal
SC1
291
h=ll)
Cord
45-60
IS THORACIC
Injury
60-75
(n=9)
75-90
Meal TIME PERIOD Figure
(minutes)
3. Colonic myoelectrical spike potential frequency from 9 patients with thoracic spinal cord injury is compared from 11 control subjects. Although normal volunteers demonstrated a postprandial increase in myoelectrical frequency (p < 0.01 vs. baseline], the patients with spinal cord injury had no response.
The colonic myoelectrical spike potential frequencies recorded in the normal controls and in the patients with spinal cord injury are shown in Figure 3. Coincident with the increase in the mean amplitude of colonic motor activity, normal control subjects demonstrated an increase in the number of spike potentials in the first 15-min interval after the meal (p < 0.02). This increase persisted through the second postprandial 15-min interval (p < 0.01). The frequency of spike potentials returned toward their preprandial levels during the third and fourth l5min postprandial periods. However, in the patients with spinal cord injury, the frequency of spike potentials did not change after the meal.
Colonic Motor and Myoelectrical Activity Response to Neostigmine Stimulation The colonic motor and myoelectrical response to the subcutaneous administration of 1 mg of neostigmine in the 6 patients with spinal cord injury studied is demonstrated in Figures 4 and 5. The patients with spinal cord injury responded to neostigmine stimulation with an increase in both motor and myoelectrical activity (p < 0.02).
with the results spike potential
Discussion The electrodiagnostic assessment of motor and sensory nerve conduction velocities is a sensitive method for the evaluation of peripheral nerve function. All of the patients with thoracic spinal cord injury demonstrated normal peripheral nerve conduction. Somatosensory-evoked responses evaluate sensory conduction in the dorsal column of the spinal cord (10,18,19). The spinal-evoked response. on stimulation of the posterior tibia1 nerve, measures the peripheral conduction time in afferent somatic: nerves between the stimulation and the recording sites. The cortical response measures the conduction time in peripheral afferent somatic nerves plus the central conduction time through the dorsal column and brain stem pathways to the sensory cortex (10,18,19). Absent cortical somatosensory-evoked responses upon stimulation of the posterior tibia1 nerve in the presence of normal spinal somatosensory-evoked responses, as seen in most of our patients with spinal cord injury, suggests a lesion within the spinal cord dorsal column pathways. The bulbocavernosus reflex response tests a reflex loop that includes both sensory and motor pudendal fibers
292
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Bas:line THORACIC
Figure
SPINAL
CORD
Post Neostigmine INJURY
PATIENTS
4. The colonic motor activity in response to parenteral injection of 1 mg of neostigmine is compared with the baseline activity in 6 patients with thoracic spinal cord injury. The patients responded to neostigmine stimulation with an increase in motor activity (p < 0.02).
and conduction through the sacral spinal cord (l517). A normal bulbocavernosus reflex response suggests integrity of the distal spinal cord, conus medullaris, and cauda equina. The measurement of spinal, cortical, and bulbocavernosus responses on stimulation of the pudendal nerve permits the evaluation of conduction in peripheral afferent, central, conus medullaris, and peripheral efferent components of this nerve. These studies demonstrate the integrity of these somatic pathways below the level of L-l, and the disruption central to L-l. Detrusor hyperreflexia is the most common cystometric disturbance described in spinal cord injury (l-5). The contraction of the urinary bladder in response to distention is mediated by a spinal reflex mechanism. In normal individuals, this reflex is inhibited by input from higher centers in the brain (21,22). The interruption of descending spinal pathways causes contractions of the bladder in the presence of smaller-than-normal degrees of organ distention and prevents voluntary suppression of these contractions (23). In our patients with spinal cord injury, the abnormal cortical somatosensory-evoked response studies and the abnormal cystometrogranrs suggest interruption of both ascending somatosensory and descending visceral pathways between the lumbar spinal cord and the cortex. The study of volume-pressure curves of the colon,
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for the characterization of neurologic disturbances, was first described in 1940 (24). These studies suggested that lesions of the motor fibers in the brain or descending spinal tracts were associated with “hyper-reflexic” or rapid-rise volume-pressure curves, whereas lesions in the sacral segments of the cauda equina or pelvic plexus caused an “areflexic” or flat volume-pressure curve. Studies in the cat (25) confirmed these observations. A recent report (7) confirmed this decrease in colonic compliance in patients with evidence of traumatic transverse thoracic spinal cord injury on clinical examination. Our patients, selected for their extensive electrodiagnostic and clinical evidence of complete thoracic spinal cord injury, confirmed these findings. The increased slope of the colonic volume pressure curves in our patients was analagous to the hyperreflexic cystosuggesting the same neuropathometrograms, physiology. To assess colonic motor activity in these patients, motor and myoelectrical activities were recorded in a resting state and after ingestion of a meal. The baseline mean amplitude of colonic motor activity in the patients with spinal cord injury was similar to that observed in the control population. However, the patients with spinal cord injury failed to demonstrate the postprandial increase in colonic motility
9-
a7
-’
6-
5-
4-
3-
2-
l-
Post
Baseline
Neostigmine THORACIC
SPINAL
CORD
INJURY
PATIENTS
The colonic myoelectrical activity in response to parenteral injection of 1 mg of neostigmine is compared with the baseline activity in 6 patients with thoracic spinal cord injury. The patients responded to neostigmine stimulation with an increase in myoelectrical activity (p i 0.02).
February
1984
observed in the control population. Spike potentials represent the electrical manifestations of smooth muscle contraction, and, hence, the myoelectrical spike potential frequency can be expected to parallel the motor activity. The baseline spike potential frequency observed in the patients with spinal cord injury was similar to that observed in the control population. However, unlike the control population, these patients with spinal cord injury failed to demonstrate a postprandial increase in spike potential frequency. Thus, these myoelectrical recordings confirmed the measurements of colonic motor activity. The motility of the pelvic colon in patients with a clinical examination compatible with injury to the thoracic spinal cord has been reported to demonstrate increased baseline activity (6). There are several explanations for the discrepancy between this previous study and our current observations. The group of patients reported by Connell (6) was a poorly defined and heterogeneous population, including patients with spinal cord injury from a variety of lesions, such as trauma, tumors, and alcohol injections. Some patients had spastic and some flaccid paralysis, and all were defined solely by physical examination rather than by electrodiagnosis. In addition, in the study reported by Connell, a different recording technique was used. Connell reported a postprandial increase in colonic motor activity in his patients with thoracic spinal cord injury. However, other studies suggest that the nervous system must be intact to mediate the postprandial colonic motor and myoelectrical response (12,26). In patients with advanced multiple sclerosis and extensive clinical and electrodiagnostic evidence of interruption of the spinal cord, the postprandial colonic response was absent (12). Lastly, the absence of the postprandial motor and myoelectrical response in diabetic patients with autonomic neuropathy and severe constipation (26) suggests that this response can be blocked by peripheral, as well as by central, nervous system dysfunction. Although several studies have suggested hormonal mediation of the postprandial colonic motor and myoelectrical response (27-29), the absent response in patients with peripheral and central nervous system dysfunction suggests that, if there is a hormonal component to this response, this hormonal component is integrated by the nervous system. Impaired gastroduodenal function cannot be implicated in the absent postprandial colonic motor and myoelectrical response in patients with diabetes mellitus or thoracic spinal cord injury. Diabetic patients with autonomic neuropathy who lacked the postprandial colonic response had normal gastric emptying (26). In addition, patients with complete thoracic spinal cord injury had normal gastric emp-
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tying and normal interdigestive antral-duodenal motor coordination (30). To exclude a myogenic component to the impaired postprandial colonic motor and myoelectrical response, we studied the colonic response to neostigmine stimulation (28,31). The increase in motor and myoelectrical activity in response to neostigmine stimulation demonstrated by our patients provides evidence for an intact myogenic component, suggesting that the absent response is neurogenic in origin. Patients with extensive clinical and electrodiagnostic evidence of somatosensory and visceral complete transverse thoracic spinal cord injury have abnormal colonic compliance and absent postprandial colonic motor and myoelectrical responses. However, these patients respond to neostigmine stimulation with a normal increase in colonic motor and myoelectrical activity, suggesting an intact myogenie component. These data suggest that the central nervous system is essential for the mediation of the postprandial colonic increase in motor and myoelectrical activity. In patients with thoracic spinal cord injury, abnormal colonic compliance and absent postprandial colonic motor and myoelectrical responses may be mediated by ablation of outflow from higher centers to the lower spinal cord and may be correlates of visceral neuropathy and severe constipation.
References 1. Bors E. Neurogenic bladder. Ural Surv 1957;7:177-250. 2. Rossier A, Bors E. Detrusor responses to perineal and rectal stimulation in patients with spinal cord injuries. Ural Int 1964;18:181-90. 3. Rossier AB, Ott R. Urinary manometry in spinal cord injury. Br J Uro1 1974;46:439-48. 4. Yalla SV, Rossier AB, Fam B. Synchronous cystosphincterometry in patients with spinal cord injury. Urology 1975: 6:777-a. 5. Yalla SV, Rossier AB, Fam B. Dyssynergic vesicourethral responses during bladder rehabilitation in spinal cord injury patients: effects of suprapubic percussion, crede method and bethanechol chloride. J Urol 1976;115:575-9. 6. Connell AM, Frankel H, Guttmenn L. The motility of the pelvic colon following complete lesions of the spinal cord. Paraplegia 1963;1:98-115. 7. Meshkinpour H, Nowroozi F, Glick ME. Colonic compliance in patients with spinal cord injury. Arch Phys Med Rehabil 1983;64:111-2. J, Eberstein A. Electrodiagnosis of neuromuscular 8. Goodgold disease. Baltimore, Md.: Williams & Wilkins, 1972. S, Bradley WE, Bhatia NN, Johnson BK. Pudendal 9. Haldeman evoked responses. Arch Neurol 1982;39:280-3. 10. Jones SJ, Small DG. Spinal and sub-cortical evoked potentials following stimulation of the posterior tibia1 nerve in man. Electroencephalogr Clin Neurophysiol 1978:44:299-306. 11. Raz S, Bradley WE. Neuromuscular dysfunction of the lower urinary tract. In: Harrison JH. Gilles RF, Perlmutter AD, et al..
294
12.
13.
14. 15.
16.
GLICK
ET AL.
eds. Cambell’s urology. Philadelphia: WB Saunders, 1979: 1215-72. Glick ME, Meshkinpour H, Haldeman S, Bhatia NN, Bradley WE. Colonic dysfunction in multiple sclerosis. Gastroenterology 1982;83:1002-7. Taylor I, Duthie HL, Smallwood R, et al. The effect of stimulation on the myoelectrical activity of the rectosigmoid in man. Gut 1974;15:599-607. Bowes A. Bowes and Church’s food values of portions commonly used. 13th ed. New York: Harper & Row, 1980. Ertekin C, Reel F. Bulbocavernosus reflex in normal men and in patients with neurogenic bladder and/or impotence. J Neurol Sci 1976;28:1-15. Dick HC, Bradley WE, Scott FB, Timm GW. Pudendal sexual reflexes: electrophysiologic investigations. Urology 1974; 3:376-g.
17. Siroky MB, Sax DS, Krane RJ. Sacral signal tracing: the electrophysiology of the bulbocavernosus reflex. J Ural 1979; 122:661-4. 18. Eisen A, Elleker G. Sensory nerve stimulation and evoked cerebral potentials. Neurology 1980;30:1097-105, 19. Cusick JF, Myklebest JB, Larson SJ, Sances A. Spinal cord evaluation by cortical evoked responses. Arch Nemo1 1979; 36:140-3. 20. Bradley WE, Chou S, Markland C. Classifying neurologic dysfunction in the urinary bladder. In: Boyarsky S, ed. The neurogenic bladder. Baltimore, Md.: Williams & Wilkins. 1967: 139-46. 21. Kuru M. Nervous control of micturition. Physiol Rev 1965: 45:425-94.
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22. Barrington FJF. The relation of the hind-brain to micturition. Brain 1921;44:23. 23. Bradley WE, Timm GW. Scott FB. Cystometry II: central nervous system organization of detrusor reflex. CJrology 1975; 5~578-80. 24. White JC, Verlot MC, Ehrentheil 0. Neurogenic disturbances of the colon and their investigation by the colonometrogram. Ann Surg 1940;112:1042-57. 25. Scott HW, Cantrell JR. Colonometrographic studies of the effects of section of the parasympathetic nerves of the colon. Bull Johns Hopkins Hosp 1949;85:310-9. 26. Battle WM, Snape WJ, Alavi A, et al. Colonic dysfunction in diabetes mellitus. Gastroenterology 1980;79:1217-21. 27. Snape WJ, Matarazoo SA, Cohen S. Effect of eating and gastrointestinal hormones on human colonic myoelectrical and motor activity. Gastroenterology 1978;75:373-8. 28. Snape WJ, Carlson GM. Cohen S. Human colonic myoelectrical activity in response to prostigmin and the gastrointestinal hormones. Am J Dig Dis 1977:22:881-8. 29. Dinoso VP, Meshkinpour H, Lorber SH. et al. Motor responses of the sigmoid colon and rectum to exogenous cholecystokinin and secretion. Gastroenterology 1973;65:438-44. 30. Fealey RD, Szurszewski JH, Merritt JL, DiMagno EP. The effect of traumatic spinal cord transection on human upper gastrointestinal motility (abstr). Gastroenterology 1982; 82:1053. 31. Chaudhary NA. Truelove SC. Human colonic motility: a comparative study of normal subjects, patients with ulcerative colitis, and patients with the irritable colon syndrome. II. The effect of prostigmin. Gastroenterology 1961;40:18-26.