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External Sphincter Dyssynergia: An Abnormal Continence Reflex
0022-5347 /88/1401-0105$2.00/0 Vol. 140, July
THE JOUR1'1AL OF UROLOGY
Copyright© 1988 by The Williams & Wilkins Co.
Printed in U.S.A.
Urological Neurology and Urodynamics EXTERNAL SPHINCTER DYSSYNERGIA: AN ABNORMAL CONTINENCE REFLEX DELBERT C. RUDY,* SAID A. AWAD
AND
JOHN W. DOWNIE
From the Departments of Urology and Pharmacology, Faculty of Medicine, Dalhausie University, Halifax, Nova Scotia, Canada ABSTRACT
Some of the characteristics of detrusor-external sphincter dyssynergia were examined in 14 patients with traumatic upper motor neuron lesions within 44 weeks of injury. The sacral evoked response latencies of the male patients were shortened at any time after injury. A continence reflex could be demonstrated in most patients at any time after injury. Comparing averaged values for the group at 4-week intervals, resting pressure at the external urethral sphincter and post-void residual volumes reached nadirs at 12 weeks while voiding efficiency peaked at this time. Thus, voiding function appears to be optimal 12 weeks after injury. During reflex detrusor activity, increases in external urethral sphincter electromyographic activity and external urethral sphincter pressure were associated clearly with a positive slope of the intravesical pressure trace, whereas decreases in both parameters were associated with a negative slope. Voiding occurred only during a negative slope. Although propantheline induced detrusor areflexia, episodic peaks in external urethral sphincter pressure and electromyographic activity continued to occur. We propose that external sphincter dyssynergia, which is independent of detrusor contraction, is the continence reflex exaggerated owing to the loss of supraspinal influences. We believe that the multiple patterns of dyssynergia described previously by others are variations, largely owing to technique, of the single pattern we have observed. The observation of synergic-like urethral responses in some patients during a negative slope of the intravesical pressure, even with complete suprasacral spinal lesions, implies existence of a pathway for synergic-like voiding in the spinal cord. (J. Ural., 140: 105-110, 1988) During the normal micturition cycle, an increase in external urethral sphincter electromyographic activity accompanies bladder filling (the continence reflex). This reflex is followed by relaxation of the external urethral sphincter, which begins before (or at the beginning of) the detrusor contraction and persists throughout the contraction.' External sphincter dyssynergia is defined as an inappropriate increase in external urethral sphincter activity during a detrusor contraction and is a well recognized cause of morbidity in patients with upper motor neuron lesions. 2 • 3 We have found that the continence reflex persists after traumatic upper motor neuron injury, complete or incomplete. We examine various characteristics of external urethral sphincter and reflex detrusor activity after suprasacrai spinal cord injury, including some evolutionary aspects, and offer a new concept of external sphincter dyssynergia associated with reflex detrusor activity. METHODS AND MATERIALS
A total of 14 consecutive patients with traumatic upper motor neuron spinal cord injuries and detrusor external sphincter dyssynergia underwent single or sequential urodynamic evaluation (table 1). Weekly neurological evaluations were performed to assess extent and level of injury in the acute spinal cord injury patients. In addition, all patients had a neurological examination to assess current extent and level of injury at the
Accepted for publication November 12, 1987. Editor's note. This paper was awarded a prize in the essay contest sponsored by the American Urological Association, May 1985. Supported by the American Urological Association Scholarship Program and by an operating grant from the Medical Council of Canada. *Requests for reprints: Texas Medical Center, 6431 Fannin St., Suite 6018, Houston, Texas 77030.
time of each urodynamic evaluation, including evaluation of perinea! sensation, clinical and electrical evaluation of the bulbocavernosus reflex, voluntary anal contraction and anal sphincter tone. A suprasacral lesion was considered complete if there was complete loss of voluntary motor function and cognitive sensory function below the level of the lesion with intact sacral cord reflex function. Urodynamic studies were performed with the patient in the supine position. External urethral sphincter electromyography was performed with a concentric needle electrode (DISA) 0.45 mm. in diameter. The electrode was positioned so that individual motor units with optimal amplitude were identified by sound and on the oscilloscope (DISA 14 All electromyograph). Electromyographic activity was recorded from the oscilloscope screen at 70 to 100 msec. sweep time at various sensitivities to quantitate the activity. Signals were amplified using an amplifier with a built-in mean value circuit (DISA 21C01). Thus, increases in electromyographic activity were depicted as increases above baseline value. Sacral evoked responses were elicited in male patients with 3 to 5 stimuli per second from surface electrodes placed on the dorsal penile shaft. The evoked electromyographic response was averaged (DISA 14Gll averager, 100 to 200 responses) and minimum latency time was determined for stimulations of 1 to 500 volts and a stimulus duration of 0.1 msec. Continuous urethral pressure profiles were performed by hand in conjunction with repeated elicitation of the bulbocavernosus reflex to locate the urethral position of the external sphincter. Resting urethral pressure at the external sphincter was defined as the pressure at this point with the catheter motionless and the electromyographic activity at baseline. Intra-abdominal pressures were not recorded. No problems were encountered with artifacts secondary to voluntary abdominal straining, since all patients had significant
106
RUDY, AWAD AND DOWNIE TABLE
Pt.-Sex-Age
Date of Injury
Level*
AF-F-32 AC-M-38 DM-M-26 MP-M-45 FA-M-36 CN-F-23 SL-M-57 JD-M-20 TR-M-26 RM-M-23 KA-M-20 KM-M-22 DR-M-23 PSt M 24
Oct. 21, 1983 Nov. 6, 1986 Oct. 10, 1983 Aug. 18, 1983 Feb. 12, 1983 Oct. 20, 1983 Oct. 16, 1983 Nov. 29, 1983 Nov. 21, 1983 Aug. 6, 1983 Oct. 21, 1983 July 24, 1983 Sept. 25, 1983 Nov. 26, 1983
CS/Tl C7/Tl T5 T6 T12 CS/Tl C7 C5/C6 C2/C3 T8/T9 T5 C5
1. Clinical data
cs
T4
Complete or Incomplete
Wks. of Urodynamic Studies From Injury
Studied After Drugs
Incomplete Incomplete Complete Incomplete Incomplete Incomplete Complete Incomplete Complete Complete Incomplete Incomplete Complete Complete
4,8, 12, 16,20 2,4,8, 16,28 18,22 16 44 1,4,8, 12,20 17, 29 1,4,8 2,4, 12 14, 18,22 1,4,8, 12,16,20 26,31,34 22 31
No Yes Yes Yes Yes Yes Yes No No No Yes Yes Yes No
. . . . . * No patient had evidence of sacral cord involvement. t Patient had a history of associated closed head injury but he was without chmcally apparent residual effects from this when evaluated. TABLE 2.
Averaged interval urodynamic parameters referenced to time from injury >20 Wks.
Resting pressure at external urethral sphincter (cm. water) Bladder capacity (ml.)* Post-void residual (ml.)* Maximum intravesical filling pressure (cm. water)* Maximum intravesical pressure with detrusor contraction (cm. water)* Maximum pressure at external urethral sphincter with detrusor contraction (cm. water)* Sacral evoked response latency (men only) (msec.) Voiding efficiency(%)*
91 ± 8
85 ± 7
77 ± 13
65 ±8
73 ± 9
79 ± 11
89±8
700±0 550±0 4±0
306 ± 134 169 ± 81 12 ± 3
354 ± 101 118 ± 12 14 ± 4
225 ± 75 74 ± 14 11 ± 1
209 ± 82 169 ± 31 14 ± 2
300 ± 61 190 ± 41 13 ± 2
291 ± 57 225 ± 23 13 ± 3
34±0
62 ± 14
85± 6
87± 4
81 ± 8
87± 6
92±4
250 ± 0
191 ± 35
152 ± 33
216 ± 33
199 ± 30
211 ± 31
211 ± 22
31.4 ± 0.9
31.9 ± 1.0
28.5 ± 0.8
31.0 ± 0.6
31.3 ± 1.3
30.3 ± 0.9
30.3 ± 0.9
21
45
67
67
19
37
23
Mean values ± standard error of the mean. * Calculated only for patients with reflex detrusor activity.
paralysis of the abdominal wall muscles. Dynamic cystosphi?cterometry consisted of simultaneous measurements of restmg external urethral sphincter pressure, intravesical pressure (10.5F microtransducer catheter) and electromyographic activity during continuous bladder filling with room te~peratu~e saline at 50 to 60 ml. per minute from a pressurized fluid reservoir. Patients were defined as having a continence reflex if electromyographic activity increased with bladder filling. Upper scale limits for intravesical and urethral pressures were 100 and 250 cm. water, respectively. Values exceeding these limits were recorded as the scale limit value. The transducers were calibrated and zeroed to atmospheric pressure at the start of each study. To avoid distension injury, no patient had greater than 700 ml. instilled into the bladder. When the initial postvoid residual was higher than the instilled volume, the postvoid residual was used as an estimation of bladder capacity. Nine patients underwent sequential same-day urodynamic studies before drug administration, 5 to 10 minutes after 5 mg. phentolamine mesylate intravenously and 30 minutes after 15 to 30 mg. propantheline bromide intramuscularly. All patients were managed acutely with intermittent catheterization on the neurosurgical ward and at the spinal cord rehabilitation center with condom catheter or indwelling Foley catheter drainage for male and female patients, respectively. Averaged urodynamic parameters were calculated for each 4week interval for the patients studied at the point of reference, from the time of injury, out to 20 weeks. Studies more than 20 weeks from the date of injury were placed in a single group. Voiding efficiency was calculated as: voiding efficiency (per cent) _ bladder capacity - post-void residual x lOO. bladder capacity
RESULTS
Areflexic and early hyperreflexic period. Averaged interval values for the parameters presented are given in table 2. On the initial study 5 patients were areflexic (all within 4 weeks of injury) and 1 had low amplitude detrusor contractions at approximately 400 ml. volume without inco?tinence (11 days aft~r injury). All 6 patients had a lower restmg electromyographic activity than normal but they showed increased activity on catheter insertion, particularly when the catheter reached the region of the external sphincter. Initially, the clinical bulbocavernosus reflex was easily detectable in 2 patients but it was weak or absent in the other 4. All patients had a prominent bulbocavernosus reflex at the subsequent urodynamic study. Initially, 5 of the 6 patients had a continence reflex although it was not marked. However, increases in total bladder pressure with filling were small as well (fig. 1). All 6 patients were dry on intermittent catheterization at this stage. Hyperreflexic period. By 8 weeks after injury, reflex detrusor activity had returned in 4 of 5 patients who initially were areflexic. All patients demonstrated dyssynergia simultaneously with the development of reflex detrusor activity. There was no meaningful trend with time from injury in the averaged maximum intravesical filling pressure, averaged maximal resting external urethral sphincter pressure with a detrusor contraction or sacral evoked response. However, averaged maximum intravesical pressures during reflex detrusor activity showed an upward trend (table 2). The averaged values of resting external urethral sphincter pressure and post-void residual reached the nadirs at i2 weeks. Voiding efficiency peaked at the 8 to 12-week interval (table 2 and fig. 2). In all 7 patients with multiple studies in the first 20 weeks after injury, reflex detrusor contractions evolved from small,
EXTERNAL SPHINCTER DYSSYNERGIA
L PVES
PURA ,.i,,
EMG w._,_,.,•·--.;...
1
t Jaatrt
11
*
r
FIG. 1. Urodynamic study of patient A. F. 4 weeks after traumatic upper motor neuron injury demonstrates continence reflex before return of reflex detrusor activity. Vertical bar represents 40 cm. water in top trace, and 16 µV. in bottom trace. Horizontal bar represents 1 minute. Dashed line represents zero on each trace. Filling begins at asterisk. PVES, intravesical pressure. PURA, pressure at external urethral sphincter. EMG, electromyography.
120
A
_ 100 ~
:c E c.:,
<(
80
\/ ····· ... :.--\\ ·. \._\
60
........ ·.--·
40
.,,., ... __
* PVES _...
M
/
/ /
\
-.-,. .-7·//-..., -:::,····,
C:
=> a.
PVES *
20 0
"cl- 100
B
80 >u 60 z LU
u
40 u:: u.. LU
C!l
z
20
PVES *
Cl
0 > 700
6
C
600 u c.:,
D Bladder Capacity
500
E::J PVR
-400 ~ 300 => .....J
PVES
§; 200 100
0 0
4 8 12 16 20 WEEKS FROM INJURY
> 20
FIG. 2. Course of vesicourethral function after suprasacral injury. Abscissa is same for all 3 panels. A, sequential external urethral sphincter pressure (PURA) determination in 7 patients. Each line represents single patient. Note downward trend first 4 weeks after injury and upward trend after approximately 12 weeks. B, mean voiding efficiency for entire group of patients. Peak occurs at 8 to 12 weeks after injury. C, mean bladder capacity and mean post-void residual (PVR) for entire group of patients reach nadirs at 16 and 12 weeks after injury, respectively.
* __J
FIG. 3. Cystometrograms show evolution of reflex detrusor activity after traumatic suprasacral injury in patient K. A. From top to bottom, times from injury are 10 days, and 4, 16 and 20 weeks. Vertical bar represents 40 cm. water. Horizontal bar represents 1 minute. Filling begins at asterisk. PVES, intravesical pressure. EMG, electromyography.
brief contractions initially upon return of reflex activity to large sustained contractions as hyperreflexia became established (fig. 3). In the later intervals durations greater than 1 minute were common, with some longer than 3 minutes.
108
RUDY, AWAD AND DOWNIE
EMG~~
A
,'\
PVES
*
- ,_
,,....,.,-,.-,
',
t
PURA.
~
EMG \ittt
-...J
h
('-, /\
PVES FIG. 4. Oscilloscope traces of spontaneous external urethral sphincter direct (not integrated) electromyographic (EMG) activity before urethral manipulation. Both traces are from same patient (T. R.). Top trace is 13 days after traumatic upper motor neuron injury. Bottom trace is 12 weeks after injury. Vertical bar represents 40 µV. on both traces. Horizontal bar represents 21 and 30 msec. for top and bottom traces, respectively.
Reflex detrusor activity was susceptible to muscarinic blockade with propantheline in 8 of 9 patients. Only the remaining patient showed a higher bladder capacity after phentolamine administration and he was not given propantheline. Electromyographic activity, resting and during bladder filling, increased as the interval from injury increased. The increase was most dramatic in patients who had reflex detrusor activity from 1 study to the next. Peak-to-peak amplitudes of biphasic action potentials recorded before urethral manipulation generally were less than 100 µ V. in the early intervals after injury. By 20 weeks, however, amplitudes in excess of 100 µ V. were common (fig. 4). Frequency of resting electromyographic activity in later intervals generally was well above the 1 to 3 per second normal range. 4 Also, recruitment on the electromyogram with a detrusor contraction increased with time from injury. The continence reflex could be identified positively in 11 of 14 patients. Propantheline-induced areflexia or hyporeflexia markedly facilitated the demonstration of a continence reflex by providing adequate filling times without detrusor activity. Pattern of dyssynergia. In ali 14 patients increased electromyographic activity and resting external urethral sphincter pressure correlated closely with a positive slope (dP /dt) of the intravesical pressure trace and were simultaneous within the limits of the recording paper speed (0.5 mm. per second). With a slope of less than zero during the detrusor contraction, the electromyographic activity and resting external urethral sphincter pressure always decreased. In 9 patients both values decreased below pre-detrusor contraction levels during negative slope episodes. Voiding always occurred in these instances. In the other 5 patients electromyographic activity and external urethral sphincter pressure decreased with a negative slope of the intravesical pressure but they remained above pre-detrusor contraction levels (fig. 5). Voiding frequently occurred in these patients but only with a negative slope. On some occasions the amount of increase in electromyographic activity and external urethral sphincter pressure appeared to correlate with the magnitude of the positive slope or the interval the positive slope was sustained. Similarly, decreases in electromyographic
B
PURA
EMG FIG. 5. Urodynamic studies in 2 patients after traumatic suprasacral spinal cord injury show that increases in external urethral sphincter pressure (PURA) and external urethral sphincter integrated electromyographic (EMG) activity occur only during positive slope of intravesical pressure trace (PVES). A, patient K. A. with negative slope PURA decreases to or below pre-detrusor contraction levels. PURA returns to initial levels after end of reflex detrusor activity. Positive bulbocavernosus reflex was done to confirm proper position of transducer at external urethral sphincter. Filling began at asterisk. B, patient T. R. PURA does not decrease to pre-detrusor contraction levels during negative slope of intravesical pressure trace. Portions of traces during initial filling phases are not included. Vertical bar represents 40 cm. water for intravesical pressure (PVES) traces, 100 cm. water for PURA traces and 40 µ V. on integrated electromyographic traces. Horizontal bar represents 1 minute.
activity and resting external urethral sphincter pressure sometimes seemed related directly to the duration of a negative slope. However, the recording paper speed used did not allow for accurate calculation of the slope of the intravesical pressure. Of the 5 patients given propantheline 4 demonstrated intermittent synchronous large peaks of resting external urethral sphincter pressure and electromyographic activity without any reflex detrusor activity, although bladder pressure was increased during filling. These urethral patterns were similar to those seen with reflex detrusor activity (fig. 6). DISCUSSION
Upper motor neuron injuries frequently are associated with detrusor-external sphincter dyssynergia. 5 The association of a persistent, although abnormal, continence reflex after such injuries is important to better understand the mechanism of dyssynergia. In cats, reflex increases in external urethral sphincter activity
EXTEH,NAL SPHIJ\ICTER DYSSYNERGIA
PVES
PU RA
v"-~~
~~ -
_L_,_
EMG
PVES
B
PURA
FIG. 6. Urodynamic studies after propantheline. A, in patient K. N. marked continence reflex is readily apparent with bladder filling. Filling begins at asterisk. B, in patient F. A. peaks of external urethral sphincter activity are present despite absence ofreflex detrusor activity. Portions of traces during initial filling phase are not included. Vertical bar represents 40 cm. water for intravesical pressure (PVES) traces, 100 cm. water for external urethral sphincter pressure (PURA) traces and 16 or 40 µV. on integrated electromyographic (EMG) trace. Horizontal bar represents 1 minute.
accompany both bladder filling and urethral distension. 6 Kum called the increase in external sphincter activity with bladder filling the "continence reflex", reserving "guarding reflex" only for the increasing external urethral sphincter activity seen with urethral distension" 1 The issue is more than semantic, since the neural pathways in these 2 reflexes are different, We have defined operationally the continence reflex as increasing external urethral sphincter electromyographic activity with bladder filling. Others using the same definition have chosen to use the term guarding reflex instead. 7 Continence reflex. The evolution of electromyographic activafter traumatic suprasacral spinal cord injury is somewhat controversial. It has been reported that the continence reflex is absent or electromyographic activity decreases with bladder filling during spinal shock. 8 However, our finding of a definite continence reflex in 4 of 5 such patients verifies an earlier report of patients acutely after traumatic suprasacral spinal cord injuries. 9 Differences in bladder filling rates and electromyographic recording sensitivity may account for some of this controversy. Our findings also corroborate previous reports of the presence of a continence reflex in patients with return of reflex detrusor activity after suprasacral spinal cord injury2 • 10 and an increase in the activity of the reflex with time after injury. 4 · 8 • 11 Inasmuch as the continence reflex persists in complete motor and sensory suprasacral cord lesions, it must be a spinal reflex. 9 Bulbocavernosus reflex and sacral evoked response. In our
109
patients the clinical bulbocavemosus reflex could be depressed markedly shortly after injury but it always became prominent within 12 to 16 weeks after injury. No such evolution occurred with the sacral evoked response" With supramaxirnal stimulation, which results in latencies of 34"6 to 40 msec. in normal men, 12 • 13 we found the evoked reflex latency to be shortened irrespective of the time from injury. Bilkey and associates also found a shortened latency in suprasacral lesions but they did not reference their findings to the interval from injury" 13 One study found the same latency in normal men and men with suprasacral spinal cord injuries. 14 However, supramaximal stimuli were not used. Therefore, when the bulbocavernosus reflex is clinically absent and when there is concern about the level of the lesion, sacral evoked response studies should be useful acutely in differentiating between upper and lower motor neuron injury in male patients. Resting external urethral sphincter pressure and reflex detrusor activity. We are unable to explain fully the etiology of the evolutionary sequence of resting external urethral sphincter pressure that we have described. Resting external urethral sphincter pressure is maintained at normal to near normal values during spinal shock. 5 ' 15 The increase in pressure after 12 weeks most likely is owing to increasing activity of striated muscle at the external urethral sphincter" 2 • 10 A decrease in the external urethral sphincter pressure before 12 weeks after injury could be owing to decreasing sympathetic activity in the urethral smooth muscle in the region of the external urethral sphincter. A decrease in isolated spinal cord sympathetic reflex activity for a few weeks after spinal cord injury has been described. 16 This trend in resting external urethral sphincter pressure, the major determinant of urethral outflow resistance in dyssynergia, readily explains the parallel trends in post-void residual, bladder capacity and, most importantly, voiding efficiency. It indicates the limitation of a single evaluation of bladder function based on these parameters in the first few months after injury. We have shown that reflex detrusor activity evolves into high amplitude detrusor contractions. We cannot determine whether the fluctuating prolonged increase in intravesical pressure secondary to reflex detrusor activity is owing to multiple closely spaced separate detrusor contractions or a single contraction with fluctuations in developed tension. However, if supraspinal centers are necessary for development of a sustained contraction, the former possibility becomes more likely. 17 External sphincter dyssynergia. Having demonstrated the preservation of the continence reflex in suprasacral cord injuries and, thus, its spinal ,v,,a,iv,,, and considering the common pattern of dyssynergia in our patients, we propose that external sphincter dyssynergia is an exaggerated continence reflex. Based on a study of 550 patients Blaivas and associates concluded that loss of continuity between the pontine mesencephalic and sacral micturition centers results in external sphincter dyssynergia. 18 We propose that loss of continuity between the sacral cord pudendal and vesical motor nuclei and the supraspinal micturition centers results in the loss of appropriate inhibition of the pudendal motor nucleus during a detrusor contraction. Maneuvers that increase intravesical pressure in dyssynergic patients are well known to aggravate the bladderexternal urethral sphincter incoordination. 5 We propose that this reflects the presence of an abnormal continence reflex. Siroky and Krane concluded that dyssynergia occurs in the absence of a continence reflex despite their description of a substantial minority of patients (30 per cent) with a continence reflex and dyssynergia. 7 Our use of propantheline markedly improved our ability to confirm the presence of a continence reflex in our patients. Consistent with our hypothesis, a decreasing intravesical pressure results in a diminution of external urethral sphincter activity. We observed a negative closure pressure (voiding) only during the negative slope of the intravesical pressure of a
110
RUDY, AWAD AND DOWNIE
PVES
- - -~
It is interesting to speculate that if the continence reflex could be abolished selectively in patients with external sphincter dyssynergia, then coordinated voiding might well ensue. However, as our patients demonstrate, this still might not provide a balanced bladder. There appears still to be another missing requirement for efficient detrusor function. Dr. R. 0. Holness, Department of Neurosurgery, assisted in the serial neurological evaluation of the patients.
REFERENCES
EMG
FIG. 7. Cystometrographic/electromyographic (EMG) study from patient P. S. after traumatic suprasacral spinal cord injury using unintegrated (direct) electromyographic recording. Although peaks of electromyographic activity correlate with positive slope on cystometrogram, it could easily be interpreted as sustained pattern of dyssynergia. Vertical bar represents 40 cm. water. Horizontal bar represents 1 minute. Filling starts at asterisk. PVES, intravesical pressure.
detrusor contraction and an associated decreasing external urethral sphincter pressure. The waxing and waning pattern of the elevated intravesical pressure and associated external sphincter activity seen with reflex detrusor activity thus accounts for the intermittent voiding pattern in dyssynergic patients. Bladder fatigue cannot be a factor in the waxing and waning of the urethral response, since the same urethral response pattern occurred with bladder filling during propantheline-induced areflexia. A possible explanation is that activity in either the bladder or pudendal motor nucleus could be episodic owing to an episodic afferent nerve input 19 or to intraspinal modulation in suprasacral lesions. Our observation that in some patients resting external urethral sphincter pressure and electromyographic activity actually decrease below pre-contraction levels during a negative slope of the intravesical pressure indicates that there may be a spinal mechanism for synergic-like external sphincter relaxation.20-22 However, this still does not result in a balanced bladder. The components necessary for sacral segmental pathways subserving an increase in external urethral sphincter activity with increasing bladder pressure as well as for depression of sphincter activity by pelvic afferent impulses have been demonstrated in the chronic spinal cat. 23 • 24 If they exist in man, as we suggest based on our observations, the mechanism governing the interplay of these 2 reflex pathways is unclear. Finally, 4 patterns of external sphincter dyssynergia have been described. 3 • 25 There is no conflict with our postulate and the type I pattern of Blaivas. Type II, the intermittent pattern, is explained by the observation that reflex detrusor-mediated intravesical pressures in our patients fluctuated. Our observation has been facilitated by the use of a microtransducer catheter for pressure recording, which has improved sensitivity and frequency-response compared to fluid perfused catheters. 26 We believe that use of integrated electromyographic recording at high sensitivity will demonstrate that the sustained pattern of dyssynergia, Blaivas type III, in reality has waxing and waning of activity that will correspond to changes in slope on the intravesical pressure trace (fig. 7). The fourth type of dyssynergia, detrusor areflexia and sphincter hyperactivity,3 is similar to what we see in our patients with muscarinic blockade.
1. Kuru, M.: Nervous control of micturition. Physiol. Rev., 45: 425, 1965. 2. Diokno, A. C., Koff, S. A. and Bender, L. F.: Periurethral striated muscle activity in neurogenic bladder dysfunction. J. Urol., 112: 743, 1974. 3. McGuire, E. J. and Brady, S.: Detrusor-sphincter dyssynergia. J. Urol., 121: 774, 1979. 4. Blaivas, J. G., Labib, K. L., Bauer, S. B. and Retik, A. B.: A new approach to electromyography of the external urethral sphincter. J. Urol., 117: 773, 1977. 5. Yalla, S. V., Rossier, A. B. and Fam, B.: Dyssynergic vesicourethral responses during bladder rehabilitation in spinal cord injury patients: effects of suprapubic percussion, Crede method and bethanechol chloride. J. Urol., 115: 575, 1976. 6. Garry, R. C., Roberts, T. D. M. and Todd, J. K.: Reflexes involving the external urethral sphincter in the cat. J. Physiol., 149: 653, 1959. 7. Siroky, M. B. and Krane, R. J.: Neurologic aspects of detrusorsphincter dyssynergia, with reference to the guarding reflex. J. Urol., 127: 953, 1982. 8. Rossier, A. B., Fam, B. A., DiBenedetto, M. and Sarkarati, M.: Urodynamics in spinal shock patients. J. Urol., 122: 783, 1979. 9. Nanninga, J. B. and Meyer, P.: Urethral sphincter activity following acute spinal cord injury. J. Urol., 123: 528, 1980. 10. DiBenedetto, M. and Yalla, S. V.: Electrodiagnosis of striated urethral sphincter dysfunction. J. Urol., 122: 361, 1979. 11. Koyanagi, T., Takamatsu, T. and Taniguchi, K.: Further characterization of the external urethral sphincter in spinal cord injury: study during spinal shock and evolution of responsiveness to alpha-adrenergic stimulation. J. Urol., 131: 1122, 1984. 12. Krane, R. J. and Siroky, M. B.: Studies on sacral-evoked potentials. J. Urol., 124: 872, 1980. 13. Bilkey, W. J., Awad, E. A. and Smith, A. D.: Clinical application of sacral reflex latency. J. Urol., 129: 1187, 1983. 14. Yalla, S. V., DiBenedetto, M., Blunt, K. J., Sethi, J.M. and Fam, B. A.: Urethral striated sphincter responses to electrobulbocavernosus stimulation. J. Urol., 119: 406, 1978. 15. Awad, S. A., Bryniak, S. R., Downie, J. W. and Twiddy, D. A. S.: Urethral pressure profile during the spinal shock stage in man: a preliminary report. J. Urol., 117: 91, 1977. 16. Mathias, C. J. and Frankel, H. L.: Clinical manifestations of malfunctioning sympathetic mechanisms in tetraplegia. J. Autonom. Nerv. System, 7: 303, 1983. 17. Bradley, W. E.: Innervation of the male urinary bladder. Urol. Clin. N. Amer., 5: 279, 1978. 18. Blaivas, J. G., Sinha, H. P., Zayed, A. A. H. and Labib, K. B.: Detrusor-external sphincter dyssynergia. J. Urol., 125: 542, 1981. 19. Downie, J. W. and Armour, J. A.: Relationship of afferent nerve activity in the pelvic plexus with pressure, length and wall strain in the urinary bladder of the cat. Soc. Neurosci. Abst., 8: 858, 1982. 20. Iwatsubo, E.: Bladder recovery in patients with traumatic cervical cord injury evaluated by voiding synchronous cystosphincterometry with uroflowmetry. J. Urol., 126: 503, 1981. 21. McGuire, E. J.: Spinal cord injury. In: Clinical Evaluation and Treatment of Neurogenic Vesical Dysfunction. Baltimore: The Williams & Wilkins Co., chapt. 6, p. 75, 1984. 22. Butler, M. R.: Patterns of bladder recovery in spinal injury evaluated by serial urodynamic observations. Urology, 11: 308, 1978. 23. DeGroat, W. D. and Ryall, R. W.: Reflexes to sacral parasympathetic neurones concerned with micturition in the cat. J. Physiol., 200: 87, 1969. 24. Rampa!, G. and Mignard, P.: Behaviour of the urethral striated sphincter and of the bladder in the chronic spinal cat. Implications at the central nervous system level. Pflugers Arch., 353: 33, 1975. 25. Blaivas, J. G., Sinha, J. P., Zayed, A. A. H. and Labib, K. B.: Detrusor-external sphincter dyssynergia: a detailed electromyographic study. J. Urol., 125: 545, 1981. 26. Asmussen, M.: Intraurethral pressure recording. A comparison between tip-transducer catheters and open-end catheters with constant flow. Scand. J. Urol. Nephrol., 10: 1, 1976.
THE JOUR1'1AL OF UROLOGY
Copyright© 1988 by The Williams & Wilkins Co.
Printed in U.S.A.
Urological Neurology and Urodynamics EXTERNAL SPHINCTER DYSSYNERGIA: AN ABNORMAL CONTINENCE REFLEX DELBERT C. RUDY,* SAID A. AWAD
AND
JOHN W. DOWNIE
From the Departments of Urology and Pharmacology, Faculty of Medicine, Dalhausie University, Halifax, Nova Scotia, Canada ABSTRACT
Some of the characteristics of detrusor-external sphincter dyssynergia were examined in 14 patients with traumatic upper motor neuron lesions within 44 weeks of injury. The sacral evoked response latencies of the male patients were shortened at any time after injury. A continence reflex could be demonstrated in most patients at any time after injury. Comparing averaged values for the group at 4-week intervals, resting pressure at the external urethral sphincter and post-void residual volumes reached nadirs at 12 weeks while voiding efficiency peaked at this time. Thus, voiding function appears to be optimal 12 weeks after injury. During reflex detrusor activity, increases in external urethral sphincter electromyographic activity and external urethral sphincter pressure were associated clearly with a positive slope of the intravesical pressure trace, whereas decreases in both parameters were associated with a negative slope. Voiding occurred only during a negative slope. Although propantheline induced detrusor areflexia, episodic peaks in external urethral sphincter pressure and electromyographic activity continued to occur. We propose that external sphincter dyssynergia, which is independent of detrusor contraction, is the continence reflex exaggerated owing to the loss of supraspinal influences. We believe that the multiple patterns of dyssynergia described previously by others are variations, largely owing to technique, of the single pattern we have observed. The observation of synergic-like urethral responses in some patients during a negative slope of the intravesical pressure, even with complete suprasacral spinal lesions, implies existence of a pathway for synergic-like voiding in the spinal cord. (J. Ural., 140: 105-110, 1988) During the normal micturition cycle, an increase in external urethral sphincter electromyographic activity accompanies bladder filling (the continence reflex). This reflex is followed by relaxation of the external urethral sphincter, which begins before (or at the beginning of) the detrusor contraction and persists throughout the contraction.' External sphincter dyssynergia is defined as an inappropriate increase in external urethral sphincter activity during a detrusor contraction and is a well recognized cause of morbidity in patients with upper motor neuron lesions. 2 • 3 We have found that the continence reflex persists after traumatic upper motor neuron injury, complete or incomplete. We examine various characteristics of external urethral sphincter and reflex detrusor activity after suprasacrai spinal cord injury, including some evolutionary aspects, and offer a new concept of external sphincter dyssynergia associated with reflex detrusor activity. METHODS AND MATERIALS
A total of 14 consecutive patients with traumatic upper motor neuron spinal cord injuries and detrusor external sphincter dyssynergia underwent single or sequential urodynamic evaluation (table 1). Weekly neurological evaluations were performed to assess extent and level of injury in the acute spinal cord injury patients. In addition, all patients had a neurological examination to assess current extent and level of injury at the
Accepted for publication November 12, 1987. Editor's note. This paper was awarded a prize in the essay contest sponsored by the American Urological Association, May 1985. Supported by the American Urological Association Scholarship Program and by an operating grant from the Medical Council of Canada. *Requests for reprints: Texas Medical Center, 6431 Fannin St., Suite 6018, Houston, Texas 77030.
time of each urodynamic evaluation, including evaluation of perinea! sensation, clinical and electrical evaluation of the bulbocavernosus reflex, voluntary anal contraction and anal sphincter tone. A suprasacral lesion was considered complete if there was complete loss of voluntary motor function and cognitive sensory function below the level of the lesion with intact sacral cord reflex function. Urodynamic studies were performed with the patient in the supine position. External urethral sphincter electromyography was performed with a concentric needle electrode (DISA) 0.45 mm. in diameter. The electrode was positioned so that individual motor units with optimal amplitude were identified by sound and on the oscilloscope (DISA 14 All electromyograph). Electromyographic activity was recorded from the oscilloscope screen at 70 to 100 msec. sweep time at various sensitivities to quantitate the activity. Signals were amplified using an amplifier with a built-in mean value circuit (DISA 21C01). Thus, increases in electromyographic activity were depicted as increases above baseline value. Sacral evoked responses were elicited in male patients with 3 to 5 stimuli per second from surface electrodes placed on the dorsal penile shaft. The evoked electromyographic response was averaged (DISA 14Gll averager, 100 to 200 responses) and minimum latency time was determined for stimulations of 1 to 500 volts and a stimulus duration of 0.1 msec. Continuous urethral pressure profiles were performed by hand in conjunction with repeated elicitation of the bulbocavernosus reflex to locate the urethral position of the external sphincter. Resting urethral pressure at the external sphincter was defined as the pressure at this point with the catheter motionless and the electromyographic activity at baseline. Intra-abdominal pressures were not recorded. No problems were encountered with artifacts secondary to voluntary abdominal straining, since all patients had significant
106
RUDY, AWAD AND DOWNIE TABLE
Pt.-Sex-Age
Date of Injury
Level*
AF-F-32 AC-M-38 DM-M-26 MP-M-45 FA-M-36 CN-F-23 SL-M-57 JD-M-20 TR-M-26 RM-M-23 KA-M-20 KM-M-22 DR-M-23 PSt M 24
Oct. 21, 1983 Nov. 6, 1986 Oct. 10, 1983 Aug. 18, 1983 Feb. 12, 1983 Oct. 20, 1983 Oct. 16, 1983 Nov. 29, 1983 Nov. 21, 1983 Aug. 6, 1983 Oct. 21, 1983 July 24, 1983 Sept. 25, 1983 Nov. 26, 1983
CS/Tl C7/Tl T5 T6 T12 CS/Tl C7 C5/C6 C2/C3 T8/T9 T5 C5
1. Clinical data
cs
T4
Complete or Incomplete
Wks. of Urodynamic Studies From Injury
Studied After Drugs
Incomplete Incomplete Complete Incomplete Incomplete Incomplete Complete Incomplete Complete Complete Incomplete Incomplete Complete Complete
4,8, 12, 16,20 2,4,8, 16,28 18,22 16 44 1,4,8, 12,20 17, 29 1,4,8 2,4, 12 14, 18,22 1,4,8, 12,16,20 26,31,34 22 31
No Yes Yes Yes Yes Yes Yes No No No Yes Yes Yes No
. . . . . * No patient had evidence of sacral cord involvement. t Patient had a history of associated closed head injury but he was without chmcally apparent residual effects from this when evaluated. TABLE 2.
Averaged interval urodynamic parameters referenced to time from injury >20 Wks.
Resting pressure at external urethral sphincter (cm. water) Bladder capacity (ml.)* Post-void residual (ml.)* Maximum intravesical filling pressure (cm. water)* Maximum intravesical pressure with detrusor contraction (cm. water)* Maximum pressure at external urethral sphincter with detrusor contraction (cm. water)* Sacral evoked response latency (men only) (msec.) Voiding efficiency(%)*
91 ± 8
85 ± 7
77 ± 13
65 ±8
73 ± 9
79 ± 11
89±8
700±0 550±0 4±0
306 ± 134 169 ± 81 12 ± 3
354 ± 101 118 ± 12 14 ± 4
225 ± 75 74 ± 14 11 ± 1
209 ± 82 169 ± 31 14 ± 2
300 ± 61 190 ± 41 13 ± 2
291 ± 57 225 ± 23 13 ± 3
34±0
62 ± 14
85± 6
87± 4
81 ± 8
87± 6
92±4
250 ± 0
191 ± 35
152 ± 33
216 ± 33
199 ± 30
211 ± 31
211 ± 22
31.4 ± 0.9
31.9 ± 1.0
28.5 ± 0.8
31.0 ± 0.6
31.3 ± 1.3
30.3 ± 0.9
30.3 ± 0.9
21
45
67
67
19
37
23
Mean values ± standard error of the mean. * Calculated only for patients with reflex detrusor activity.
paralysis of the abdominal wall muscles. Dynamic cystosphi?cterometry consisted of simultaneous measurements of restmg external urethral sphincter pressure, intravesical pressure (10.5F microtransducer catheter) and electromyographic activity during continuous bladder filling with room te~peratu~e saline at 50 to 60 ml. per minute from a pressurized fluid reservoir. Patients were defined as having a continence reflex if electromyographic activity increased with bladder filling. Upper scale limits for intravesical and urethral pressures were 100 and 250 cm. water, respectively. Values exceeding these limits were recorded as the scale limit value. The transducers were calibrated and zeroed to atmospheric pressure at the start of each study. To avoid distension injury, no patient had greater than 700 ml. instilled into the bladder. When the initial postvoid residual was higher than the instilled volume, the postvoid residual was used as an estimation of bladder capacity. Nine patients underwent sequential same-day urodynamic studies before drug administration, 5 to 10 minutes after 5 mg. phentolamine mesylate intravenously and 30 minutes after 15 to 30 mg. propantheline bromide intramuscularly. All patients were managed acutely with intermittent catheterization on the neurosurgical ward and at the spinal cord rehabilitation center with condom catheter or indwelling Foley catheter drainage for male and female patients, respectively. Averaged urodynamic parameters were calculated for each 4week interval for the patients studied at the point of reference, from the time of injury, out to 20 weeks. Studies more than 20 weeks from the date of injury were placed in a single group. Voiding efficiency was calculated as: voiding efficiency (per cent) _ bladder capacity - post-void residual x lOO. bladder capacity
RESULTS
Areflexic and early hyperreflexic period. Averaged interval values for the parameters presented are given in table 2. On the initial study 5 patients were areflexic (all within 4 weeks of injury) and 1 had low amplitude detrusor contractions at approximately 400 ml. volume without inco?tinence (11 days aft~r injury). All 6 patients had a lower restmg electromyographic activity than normal but they showed increased activity on catheter insertion, particularly when the catheter reached the region of the external sphincter. Initially, the clinical bulbocavernosus reflex was easily detectable in 2 patients but it was weak or absent in the other 4. All patients had a prominent bulbocavernosus reflex at the subsequent urodynamic study. Initially, 5 of the 6 patients had a continence reflex although it was not marked. However, increases in total bladder pressure with filling were small as well (fig. 1). All 6 patients were dry on intermittent catheterization at this stage. Hyperreflexic period. By 8 weeks after injury, reflex detrusor activity had returned in 4 of 5 patients who initially were areflexic. All patients demonstrated dyssynergia simultaneously with the development of reflex detrusor activity. There was no meaningful trend with time from injury in the averaged maximum intravesical filling pressure, averaged maximal resting external urethral sphincter pressure with a detrusor contraction or sacral evoked response. However, averaged maximum intravesical pressures during reflex detrusor activity showed an upward trend (table 2). The averaged values of resting external urethral sphincter pressure and post-void residual reached the nadirs at i2 weeks. Voiding efficiency peaked at the 8 to 12-week interval (table 2 and fig. 2). In all 7 patients with multiple studies in the first 20 weeks after injury, reflex detrusor contractions evolved from small,
EXTERNAL SPHINCTER DYSSYNERGIA
L PVES
PURA ,.i,,
EMG w._,_,.,•·--.;...
1
t Jaatrt
11
*
r
FIG. 1. Urodynamic study of patient A. F. 4 weeks after traumatic upper motor neuron injury demonstrates continence reflex before return of reflex detrusor activity. Vertical bar represents 40 cm. water in top trace, and 16 µV. in bottom trace. Horizontal bar represents 1 minute. Dashed line represents zero on each trace. Filling begins at asterisk. PVES, intravesical pressure. PURA, pressure at external urethral sphincter. EMG, electromyography.
120
A
_ 100 ~
:c E c.:,
<(
80
\/ ····· ... :.--\\ ·. \._\
60
........ ·.--·
40
.,,., ... __
* PVES _...
M
/
/ /
\
-.-,. .-7·//-..., -:::,····,
C:
=> a.
PVES *
20 0
"cl- 100
B
80 >u 60 z LU
u
40 u:: u.. LU
C!l
z
20
PVES *
Cl
0 > 700
6
C
600 u c.:,
D Bladder Capacity
500
E::J PVR
-400 ~ 300 => .....J
PVES
§; 200 100
0 0
4 8 12 16 20 WEEKS FROM INJURY
> 20
FIG. 2. Course of vesicourethral function after suprasacral injury. Abscissa is same for all 3 panels. A, sequential external urethral sphincter pressure (PURA) determination in 7 patients. Each line represents single patient. Note downward trend first 4 weeks after injury and upward trend after approximately 12 weeks. B, mean voiding efficiency for entire group of patients. Peak occurs at 8 to 12 weeks after injury. C, mean bladder capacity and mean post-void residual (PVR) for entire group of patients reach nadirs at 16 and 12 weeks after injury, respectively.
* __J
FIG. 3. Cystometrograms show evolution of reflex detrusor activity after traumatic suprasacral injury in patient K. A. From top to bottom, times from injury are 10 days, and 4, 16 and 20 weeks. Vertical bar represents 40 cm. water. Horizontal bar represents 1 minute. Filling begins at asterisk. PVES, intravesical pressure. EMG, electromyography.
brief contractions initially upon return of reflex activity to large sustained contractions as hyperreflexia became established (fig. 3). In the later intervals durations greater than 1 minute were common, with some longer than 3 minutes.
108
RUDY, AWAD AND DOWNIE
EMG~~
A
,'\
PVES
*
- ,_
,,....,.,-,.-,
',
t
PURA.
~
EMG \ittt
-...J
h
('-, /\
PVES FIG. 4. Oscilloscope traces of spontaneous external urethral sphincter direct (not integrated) electromyographic (EMG) activity before urethral manipulation. Both traces are from same patient (T. R.). Top trace is 13 days after traumatic upper motor neuron injury. Bottom trace is 12 weeks after injury. Vertical bar represents 40 µV. on both traces. Horizontal bar represents 21 and 30 msec. for top and bottom traces, respectively.
Reflex detrusor activity was susceptible to muscarinic blockade with propantheline in 8 of 9 patients. Only the remaining patient showed a higher bladder capacity after phentolamine administration and he was not given propantheline. Electromyographic activity, resting and during bladder filling, increased as the interval from injury increased. The increase was most dramatic in patients who had reflex detrusor activity from 1 study to the next. Peak-to-peak amplitudes of biphasic action potentials recorded before urethral manipulation generally were less than 100 µ V. in the early intervals after injury. By 20 weeks, however, amplitudes in excess of 100 µ V. were common (fig. 4). Frequency of resting electromyographic activity in later intervals generally was well above the 1 to 3 per second normal range. 4 Also, recruitment on the electromyogram with a detrusor contraction increased with time from injury. The continence reflex could be identified positively in 11 of 14 patients. Propantheline-induced areflexia or hyporeflexia markedly facilitated the demonstration of a continence reflex by providing adequate filling times without detrusor activity. Pattern of dyssynergia. In ali 14 patients increased electromyographic activity and resting external urethral sphincter pressure correlated closely with a positive slope (dP /dt) of the intravesical pressure trace and were simultaneous within the limits of the recording paper speed (0.5 mm. per second). With a slope of less than zero during the detrusor contraction, the electromyographic activity and resting external urethral sphincter pressure always decreased. In 9 patients both values decreased below pre-detrusor contraction levels during negative slope episodes. Voiding always occurred in these instances. In the other 5 patients electromyographic activity and external urethral sphincter pressure decreased with a negative slope of the intravesical pressure but they remained above pre-detrusor contraction levels (fig. 5). Voiding frequently occurred in these patients but only with a negative slope. On some occasions the amount of increase in electromyographic activity and external urethral sphincter pressure appeared to correlate with the magnitude of the positive slope or the interval the positive slope was sustained. Similarly, decreases in electromyographic
B
PURA
EMG FIG. 5. Urodynamic studies in 2 patients after traumatic suprasacral spinal cord injury show that increases in external urethral sphincter pressure (PURA) and external urethral sphincter integrated electromyographic (EMG) activity occur only during positive slope of intravesical pressure trace (PVES). A, patient K. A. with negative slope PURA decreases to or below pre-detrusor contraction levels. PURA returns to initial levels after end of reflex detrusor activity. Positive bulbocavernosus reflex was done to confirm proper position of transducer at external urethral sphincter. Filling began at asterisk. B, patient T. R. PURA does not decrease to pre-detrusor contraction levels during negative slope of intravesical pressure trace. Portions of traces during initial filling phases are not included. Vertical bar represents 40 cm. water for intravesical pressure (PVES) traces, 100 cm. water for PURA traces and 40 µ V. on integrated electromyographic traces. Horizontal bar represents 1 minute.
activity and resting external urethral sphincter pressure sometimes seemed related directly to the duration of a negative slope. However, the recording paper speed used did not allow for accurate calculation of the slope of the intravesical pressure. Of the 5 patients given propantheline 4 demonstrated intermittent synchronous large peaks of resting external urethral sphincter pressure and electromyographic activity without any reflex detrusor activity, although bladder pressure was increased during filling. These urethral patterns were similar to those seen with reflex detrusor activity (fig. 6). DISCUSSION
Upper motor neuron injuries frequently are associated with detrusor-external sphincter dyssynergia. 5 The association of a persistent, although abnormal, continence reflex after such injuries is important to better understand the mechanism of dyssynergia. In cats, reflex increases in external urethral sphincter activity
EXTEH,NAL SPHIJ\ICTER DYSSYNERGIA
PVES
PU RA
v"-~~
~~ -
_L_,_
EMG
PVES
B
PURA
FIG. 6. Urodynamic studies after propantheline. A, in patient K. N. marked continence reflex is readily apparent with bladder filling. Filling begins at asterisk. B, in patient F. A. peaks of external urethral sphincter activity are present despite absence ofreflex detrusor activity. Portions of traces during initial filling phase are not included. Vertical bar represents 40 cm. water for intravesical pressure (PVES) traces, 100 cm. water for external urethral sphincter pressure (PURA) traces and 16 or 40 µV. on integrated electromyographic (EMG) trace. Horizontal bar represents 1 minute.
accompany both bladder filling and urethral distension. 6 Kum called the increase in external sphincter activity with bladder filling the "continence reflex", reserving "guarding reflex" only for the increasing external urethral sphincter activity seen with urethral distension" 1 The issue is more than semantic, since the neural pathways in these 2 reflexes are different, We have defined operationally the continence reflex as increasing external urethral sphincter electromyographic activity with bladder filling. Others using the same definition have chosen to use the term guarding reflex instead. 7 Continence reflex. The evolution of electromyographic activafter traumatic suprasacral spinal cord injury is somewhat controversial. It has been reported that the continence reflex is absent or electromyographic activity decreases with bladder filling during spinal shock. 8 However, our finding of a definite continence reflex in 4 of 5 such patients verifies an earlier report of patients acutely after traumatic suprasacral spinal cord injuries. 9 Differences in bladder filling rates and electromyographic recording sensitivity may account for some of this controversy. Our findings also corroborate previous reports of the presence of a continence reflex in patients with return of reflex detrusor activity after suprasacral spinal cord injury2 • 10 and an increase in the activity of the reflex with time after injury. 4 · 8 • 11 Inasmuch as the continence reflex persists in complete motor and sensory suprasacral cord lesions, it must be a spinal reflex. 9 Bulbocavernosus reflex and sacral evoked response. In our
109
patients the clinical bulbocavemosus reflex could be depressed markedly shortly after injury but it always became prominent within 12 to 16 weeks after injury. No such evolution occurred with the sacral evoked response" With supramaxirnal stimulation, which results in latencies of 34"6 to 40 msec. in normal men, 12 • 13 we found the evoked reflex latency to be shortened irrespective of the time from injury. Bilkey and associates also found a shortened latency in suprasacral lesions but they did not reference their findings to the interval from injury" 13 One study found the same latency in normal men and men with suprasacral spinal cord injuries. 14 However, supramaximal stimuli were not used. Therefore, when the bulbocavernosus reflex is clinically absent and when there is concern about the level of the lesion, sacral evoked response studies should be useful acutely in differentiating between upper and lower motor neuron injury in male patients. Resting external urethral sphincter pressure and reflex detrusor activity. We are unable to explain fully the etiology of the evolutionary sequence of resting external urethral sphincter pressure that we have described. Resting external urethral sphincter pressure is maintained at normal to near normal values during spinal shock. 5 ' 15 The increase in pressure after 12 weeks most likely is owing to increasing activity of striated muscle at the external urethral sphincter" 2 • 10 A decrease in the external urethral sphincter pressure before 12 weeks after injury could be owing to decreasing sympathetic activity in the urethral smooth muscle in the region of the external urethral sphincter. A decrease in isolated spinal cord sympathetic reflex activity for a few weeks after spinal cord injury has been described. 16 This trend in resting external urethral sphincter pressure, the major determinant of urethral outflow resistance in dyssynergia, readily explains the parallel trends in post-void residual, bladder capacity and, most importantly, voiding efficiency. It indicates the limitation of a single evaluation of bladder function based on these parameters in the first few months after injury. We have shown that reflex detrusor activity evolves into high amplitude detrusor contractions. We cannot determine whether the fluctuating prolonged increase in intravesical pressure secondary to reflex detrusor activity is owing to multiple closely spaced separate detrusor contractions or a single contraction with fluctuations in developed tension. However, if supraspinal centers are necessary for development of a sustained contraction, the former possibility becomes more likely. 17 External sphincter dyssynergia. Having demonstrated the preservation of the continence reflex in suprasacral cord injuries and, thus, its spinal ,v,,a,iv,,, and considering the common pattern of dyssynergia in our patients, we propose that external sphincter dyssynergia is an exaggerated continence reflex. Based on a study of 550 patients Blaivas and associates concluded that loss of continuity between the pontine mesencephalic and sacral micturition centers results in external sphincter dyssynergia. 18 We propose that loss of continuity between the sacral cord pudendal and vesical motor nuclei and the supraspinal micturition centers results in the loss of appropriate inhibition of the pudendal motor nucleus during a detrusor contraction. Maneuvers that increase intravesical pressure in dyssynergic patients are well known to aggravate the bladderexternal urethral sphincter incoordination. 5 We propose that this reflects the presence of an abnormal continence reflex. Siroky and Krane concluded that dyssynergia occurs in the absence of a continence reflex despite their description of a substantial minority of patients (30 per cent) with a continence reflex and dyssynergia. 7 Our use of propantheline markedly improved our ability to confirm the presence of a continence reflex in our patients. Consistent with our hypothesis, a decreasing intravesical pressure results in a diminution of external urethral sphincter activity. We observed a negative closure pressure (voiding) only during the negative slope of the intravesical pressure of a
110
RUDY, AWAD AND DOWNIE
PVES
- - -~
It is interesting to speculate that if the continence reflex could be abolished selectively in patients with external sphincter dyssynergia, then coordinated voiding might well ensue. However, as our patients demonstrate, this still might not provide a balanced bladder. There appears still to be another missing requirement for efficient detrusor function. Dr. R. 0. Holness, Department of Neurosurgery, assisted in the serial neurological evaluation of the patients.
REFERENCES
EMG
FIG. 7. Cystometrographic/electromyographic (EMG) study from patient P. S. after traumatic suprasacral spinal cord injury using unintegrated (direct) electromyographic recording. Although peaks of electromyographic activity correlate with positive slope on cystometrogram, it could easily be interpreted as sustained pattern of dyssynergia. Vertical bar represents 40 cm. water. Horizontal bar represents 1 minute. Filling starts at asterisk. PVES, intravesical pressure.
detrusor contraction and an associated decreasing external urethral sphincter pressure. The waxing and waning pattern of the elevated intravesical pressure and associated external sphincter activity seen with reflex detrusor activity thus accounts for the intermittent voiding pattern in dyssynergic patients. Bladder fatigue cannot be a factor in the waxing and waning of the urethral response, since the same urethral response pattern occurred with bladder filling during propantheline-induced areflexia. A possible explanation is that activity in either the bladder or pudendal motor nucleus could be episodic owing to an episodic afferent nerve input 19 or to intraspinal modulation in suprasacral lesions. Our observation that in some patients resting external urethral sphincter pressure and electromyographic activity actually decrease below pre-contraction levels during a negative slope of the intravesical pressure indicates that there may be a spinal mechanism for synergic-like external sphincter relaxation.20-22 However, this still does not result in a balanced bladder. The components necessary for sacral segmental pathways subserving an increase in external urethral sphincter activity with increasing bladder pressure as well as for depression of sphincter activity by pelvic afferent impulses have been demonstrated in the chronic spinal cat. 23 • 24 If they exist in man, as we suggest based on our observations, the mechanism governing the interplay of these 2 reflex pathways is unclear. Finally, 4 patterns of external sphincter dyssynergia have been described. 3 • 25 There is no conflict with our postulate and the type I pattern of Blaivas. Type II, the intermittent pattern, is explained by the observation that reflex detrusor-mediated intravesical pressures in our patients fluctuated. Our observation has been facilitated by the use of a microtransducer catheter for pressure recording, which has improved sensitivity and frequency-response compared to fluid perfused catheters. 26 We believe that use of integrated electromyographic recording at high sensitivity will demonstrate that the sustained pattern of dyssynergia, Blaivas type III, in reality has waxing and waning of activity that will correspond to changes in slope on the intravesical pressure trace (fig. 7). The fourth type of dyssynergia, detrusor areflexia and sphincter hyperactivity,3 is similar to what we see in our patients with muscarinic blockade.
1. Kuru, M.: Nervous control of micturition. Physiol. Rev., 45: 425, 1965. 2. Diokno, A. C., Koff, S. A. and Bender, L. F.: Periurethral striated muscle activity in neurogenic bladder dysfunction. J. Urol., 112: 743, 1974. 3. McGuire, E. J. and Brady, S.: Detrusor-sphincter dyssynergia. J. Urol., 121: 774, 1979. 4. Blaivas, J. G., Labib, K. L., Bauer, S. B. and Retik, A. B.: A new approach to electromyography of the external urethral sphincter. J. Urol., 117: 773, 1977. 5. Yalla, S. V., Rossier, A. B. and Fam, B.: Dyssynergic vesicourethral responses during bladder rehabilitation in spinal cord injury patients: effects of suprapubic percussion, Crede method and bethanechol chloride. J. Urol., 115: 575, 1976. 6. Garry, R. C., Roberts, T. D. M. and Todd, J. K.: Reflexes involving the external urethral sphincter in the cat. J. Physiol., 149: 653, 1959. 7. Siroky, M. B. and Krane, R. J.: Neurologic aspects of detrusorsphincter dyssynergia, with reference to the guarding reflex. J. Urol., 127: 953, 1982. 8. Rossier, A. B., Fam, B. A., DiBenedetto, M. and Sarkarati, M.: Urodynamics in spinal shock patients. J. Urol., 122: 783, 1979. 9. Nanninga, J. B. and Meyer, P.: Urethral sphincter activity following acute spinal cord injury. J. Urol., 123: 528, 1980. 10. DiBenedetto, M. and Yalla, S. V.: Electrodiagnosis of striated urethral sphincter dysfunction. J. Urol., 122: 361, 1979. 11. Koyanagi, T., Takamatsu, T. and Taniguchi, K.: Further characterization of the external urethral sphincter in spinal cord injury: study during spinal shock and evolution of responsiveness to alpha-adrenergic stimulation. J. Urol., 131: 1122, 1984. 12. Krane, R. J. and Siroky, M. B.: Studies on sacral-evoked potentials. J. Urol., 124: 872, 1980. 13. Bilkey, W. J., Awad, E. A. and Smith, A. D.: Clinical application of sacral reflex latency. J. Urol., 129: 1187, 1983. 14. Yalla, S. V., DiBenedetto, M., Blunt, K. J., Sethi, J.M. and Fam, B. A.: Urethral striated sphincter responses to electrobulbocavernosus stimulation. J. Urol., 119: 406, 1978. 15. Awad, S. A., Bryniak, S. R., Downie, J. W. and Twiddy, D. A. S.: Urethral pressure profile during the spinal shock stage in man: a preliminary report. J. Urol., 117: 91, 1977. 16. Mathias, C. J. and Frankel, H. L.: Clinical manifestations of malfunctioning sympathetic mechanisms in tetraplegia. J. Autonom. Nerv. System, 7: 303, 1983. 17. Bradley, W. E.: Innervation of the male urinary bladder. Urol. Clin. N. Amer., 5: 279, 1978. 18. Blaivas, J. G., Sinha, H. P., Zayed, A. A. H. and Labib, K. B.: Detrusor-external sphincter dyssynergia. J. Urol., 125: 542, 1981. 19. Downie, J. W. and Armour, J. A.: Relationship of afferent nerve activity in the pelvic plexus with pressure, length and wall strain in the urinary bladder of the cat. Soc. Neurosci. Abst., 8: 858, 1982. 20. Iwatsubo, E.: Bladder recovery in patients with traumatic cervical cord injury evaluated by voiding synchronous cystosphincterometry with uroflowmetry. J. Urol., 126: 503, 1981. 21. McGuire, E. J.: Spinal cord injury. In: Clinical Evaluation and Treatment of Neurogenic Vesical Dysfunction. Baltimore: The Williams & Wilkins Co., chapt. 6, p. 75, 1984. 22. Butler, M. R.: Patterns of bladder recovery in spinal injury evaluated by serial urodynamic observations. Urology, 11: 308, 1978. 23. DeGroat, W. D. and Ryall, R. W.: Reflexes to sacral parasympathetic neurones concerned with micturition in the cat. J. Physiol., 200: 87, 1969. 24. Rampa!, G. and Mignard, P.: Behaviour of the urethral striated sphincter and of the bladder in the chronic spinal cat. Implications at the central nervous system level. Pflugers Arch., 353: 33, 1975. 25. Blaivas, J. G., Sinha, J. P., Zayed, A. A. H. and Labib, K. B.: Detrusor-external sphincter dyssynergia: a detailed electromyographic study. J. Urol., 125: 545, 1981. 26. Asmussen, M.: Intraurethral pressure recording. A comparison between tip-transducer catheters and open-end catheters with constant flow. Scand. J. Urol. Nephrol., 10: 1, 1976.