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Clinical correlation of urodynamic findings in patients with localized partial lesions of the spinal cord and cauda equina
148
Surg Neurol 1984;21:148-54
Clinical Correlation of Urodynamic Findings in Patients with Localized Partial Lesions of the Spinal Cord and Cauda Equina W . S. L. G u n a s e k e r a , I. D . E v e r s d e n ,
F . R . C . S . , A. E. R i c h a r d s o n ,
F.R.C.S., K. N. Senevirame,
Ph.D.,
and
M.Phil.
Departments of Neurosurgery and Physiology, Atkinson Morley's Hospital, London, England
Gunasekera WSL, Richardson AE, Senevirame KN, Eversden ID. Clinical correlation of urodynamic findings in patients with localized partial lesions of the spinal cord and cauda equina. Surg Neurol 1984;21:148-54. Urodynamic studies were undertaken in 70 patients with incomplete, confirmed, localized lesions involving the spinal cord and cauda equina, irrespective of clinically evident bladder disturbances. Both detrusor and urethral function were simultaneously evaluated and correlated with neurological deficits and symptoms of lower urinary tract dysfunction. It was evident that in those patients with localized spinal cord lesions, lower urinary tract disturbances were closely associated with disturbances of pinprick sensation. Clinically silent bladder and sphincter dysfunction was encountered in 14% of the patients, and the number of asymptomatic patients was significantly higher among those with upper motor neuron lesions. Incontinence was associated predominantly with conus lesions; however, the other symptoms had no relationship to the site of the lesion. Symptoms such as urgency, incontinence, and nocturnal incontinence were associated with detrusor hyperactivity, and urinary retention was associated with urethral overactivity and dyssynergia. The urodynamic findings could explain the pathogenesis of the symptoms in most instances, but were not necessarily related to them. It is concluded that the pathways subserving lower-urinary-tract function are closely associated with the pathways subserving pinprick sensation, and that a lesion along the spinal axis can affect the bladder, sphincter, or both in a variety of ways, thus leading to the widely variable clinical findings associated with neurogenic lower urinary tract dysfunction. KEYWORDS: Spinal cord; Localized partial lesions; Neurogenic bladder; Neurological deficits; Urinary symptoms; Urodynamic studies; Cauda equina
Address reprint requests to." Mr. A.E. Richardson, F.R.C.S., Consultant Neurosurgeon, Atkinson Morley's Hospital, 31 Copse Hill, Wimbledon, London S.W. ZO ONE, England. Dr. Gunasekera's present address is: Neurosurgical Unit, General Hospital, Kandy, Sri Lanka. Dr. Senevirame's present address is: Department of Physiology, Faculty of Medicine, Colombo, Sri Lanka.
© 1984 by ElsevierSciencePublishingCo., Inc.
The urodynamic assessment o f patients with neurogenic bladder disturbances has led to a better understanding of the pathophysiology o f the lower urinary tract, as well as contributing to patient management. Urodynamic studies have also been helpful in demonstrating such problems in patients with neurological disease who have otherwise had no symptomatic evidence o f such disturbances. R o s o m o f f et al found that among 100 consecutive cases of confirmed lumbar disk protrusion, only 13% had symptoms of lower urinary tract dysfunction, whereas 8 3 % had abnormalities demonstrated by urodynamic assessment [10]. The aim of this study was to evaluate lower-urinarytract function in patients with commonly occurring, localized partial lesions of the spinal cord and cauda equina, and to correlate the urodynamic findings with the clinical manifestations in this population.
Material and Methods Seventy patients with localized lesions o f the spinal cord and cauda equina, demonstrated by myelography and subsequently confirmed at operation, were studied. There were 52 males and 18 females aged from 1 9 - 7 6 years, with a mean age of 43.1 years. T h e pathology of the lesions in this group included cervical spondylosis with posterior osteophytes, spinal-cord injuries, extra- and intradural tumors, prolapsed intervertebral disks, arteriovenous malformations of the spinal cord, and spina bifida with lipomas of the conus or diastomatomyelia. The patients were clinically evaluated* in relation to any urologic disturbances and neurological manifestations, and urodynamic studies were done on all of those with myelographically demonstrable lesions, irrespective of their urologic symptoms. Prior to urodynamic study, the patients were requested to e m p t y their blad-
*Methods, definitions, and units conform to the standards recommended by the International Continence Society, except where specifically mentioned. 0090-3019/84/$3.00
Urodynamic Findings with Spinal Lesions
ders. D e t r u s o r function was evaluated by cystometry with the patient in the supine position, using sterile normal saline at r o o m temperature, infused at a constant rate of 15 mL/min via a periurethral flexible nylon catheter of 1.0 m m external diameter (Portex, Ltd.), using a p u m p to maintain the necessary pressure head. T h e intravesical pressure was recorded via another, similar catheter lying alongside the first and connected to an external pressure transducer (Statham P 37). The intraabdominal pressure was simultaneously recorded via a fluid-filled rectal catheter, and this pressure was electronically subtracted from the intravesical pressure to indicate the detrusor pressure. T h e infusion was continued until patient tolerance was reached or until leakage occurred. T h e patients were then requested to void in the supine or seated position with the catheters in situ, in order to obtain a voiding cystometrogram. Any remaining fluid was evacuated and the residual urine volume was calculated by subtracting the voided and evacuated volumes from the volume infused. Urethral function was assessed by electromyographic studies of the perianal muscles using a percutaneous coaxial needle electrode inserted anterior to the anal orifice. The intravesical pressure, the intraabdominal pressure, the detrusor pressure, and the electromyogram were simultaneously recorded during filling and voiding, using a multichannel recorder. N o complications resulted from any of these procedures. From these measurements it was possible to evaluate bladder sensation, bladder compliance, detrusor contractility, the m a x i m u m cystometric capacity, the volume of residual urine, and urethral function. Bladder sensation was assessed subjectively, guided by the infusion volume at which the first desire to void was felt, and was considered normal if the desire to void appeared when the volume infused was between 100 mL and 300 mL; increased if the volume was less than 100 mL; and reduced if the volume was over 300 mL. Patients who became incontinent without a desire to void before 300 mL had been infused were also considered as having reduced sensation. Bladder compliance, C, was measured as the change of volume, AV, per unit increase in detrusor pressure, P, during filling (i.e., C = V/P). In a normal bladder, the capacity of which is usually below 500 mL, the increase in detrusor pressure occurs between 5 and 15 c m H 2 0 at m a x i m u m cystometric capacity, and the compliance was therefore considered normal if this pressure increase occurred between 5 and 15 c m H 2 0 ; reduced if it occurred at a pressure above 15 c m H 2 0 ; and increased if it occurred at a pressure below 5 c m H 2 0 . Detrusor contractility was considered normal if no sudden increases in detrusor pressure occurred during filling, and increased pressure occurred only with vol-
Surg Neurol 1984;21:148-54
149
untarily initiated voiding. If sudden increases in detrusor pressure occurred that the patient was unable to suppress they were considered as representing hyperreflexic contractility. If no voiding-pressure increase occurred in a bladder which was also abnormal in sensation or compliance, the contractility was classified as areflexic, and if a patient with normal sensation or compliance failed to initiate voiding, the detrusor was classified as noncontractile. The maximum cystometric capacity that the patient would tolerate was classified as normal if the volume of saline infused was between 150 and 500 mL; reduced if the volume was below 150 mL; and increased if the volume was over 500 mL. A residual urine volume of 10% greater than the maximum cystometric capacity was considered significant, and a volume below this value was considered as nonsignificant. The urethra was classified as normal or overactive according to the change in amplitude on the electromyogram during filling; dyssynergic if increased electromyographic activity occurred during attempted voiding; and incompetent if fluid leakage occurred without any increase in detrusor pressure. The symptoms of lower urinary tract dysfunction, and the urodynamic findings in each case, were then analyzed in relation to the site of the lesion and the neurological deficits.
Results There were 19 patients with cervical lesions, 15 with dorsal lesions, 23 with conus lesions, and 13 with cauda equina lesions. Lesions between D-10 and L-2 were classified as conus lesions. Patients with cervical and dorsal lesions had neurological signs of u p p e r m o t o r neuron dysfunction while those with conus and cauda equina lesions had signs of lower m o t o r neuron disturbance. There was a tendency for the proportion of patients with lower urinary tract dysfunction to increase as the site of the lesion descended, with the incidence of such dysfunction increasing from 4 7 . 4 % in patients with cervical lesions to 100% in those with cauda equina lesions (Table 1); however, this last figure may be an exaggeration, as there was an unintentional tendency to undertake urodynamic studies on patients with symptomatic bladder dysfunction in this particular group. Urodynamic assessment revealed that about half of the asymptomatic patients had abnormal lower urinary tract function. Abnormal urodynamic function was found in all of the patients with lower m o t o r neuron lesions, as compared to 76.4% of those with upper m o t o r neuron lesions; however, the difference was not statistically significant. T h e r e were eight patients with u p p e r m o t o r neuron lesions who had normal bladder and sphincter
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Gunasekera et al
Table 1. Distribution of Lower Urinary Tract Function by Site of the Lesion Lower motor neuron
Upper motor neuron
Function
Cervical
Dorsal
Total in each group Asymptomatic Asymptomatic and normal function Asymptomatic but abnormal function Symptomatic and abnormal function Total urodynamic abnormalities
19 10 (52.6) a 6
15 5 (33.3) 2
4
Conus
Cauda equina
23 3 (13) 0
3
3
Total
13 0 0
70 18 (25.7) 8 (11.4)
0
10 14.2)
9 (47.4)
10 (66.6)
20 (87)
13 (100)
52 (74.3)
13 (68.4)
13 (86.7)
23 (100)
13 (100)
62 (88.6)
~Figures within parentheses represent percentages in each group
function, whereas none of those with lower motor neuron lesions had normal lower urinary tract function. In order to evaluate the relationship between lower urinary tract function and signs of neurological dysfunction, the patients were divided into four groups. Group 1 comprised eight patients who had pyramidal weakness only, and no disturbance of pinprick sensation, while group 2 comprised 12 patients with impaired pinprick sensation only and no motor deficits. In group 3 there were 28 patients who had pyramidal weakness and impaired pinprick sensation below the level of the lesion, and in group 4 there were 22 patients who had segmental weakness and impaired pinprick sensation. None of the patients in group 1 had any symptoms of lower urinary tract dysfunction, while all of those in group 2 had such symptoms (Table 2). The symptoms were most frequent among those with sensory loss only (100%), and least frequent among those with pyramidal weakness and sensory impairment (71.4%). Upon urodynamic assessment, all of the patients in group 1 were found to have normal lower urinary tract function, while all of those in groups 2, 3, and 4 had
T a b l e 2.
abnormal function. Thus, all of those with normal pinprick sensation had normal lower urinary tract function, whereas all of those with impaired pinprick sensation had abnormal lower urinary tract function. The sensory impairment in the patients with abnormal lower urinary tract function was not limited to the sacral dermatomes, extending--in some patients--to a level in the trunk corresponding to the level of the lesion. The various symptoms of lower urinary tract function were next analyzed in relation to the site of the lesion (Figure 1). Incontinence and nocturnal incontinence were seen in significantly higher proportions in patients with conus lesions (p = < 0.005), but there was no relationship between any of the other symptoms and the site of the lesion. None of the symptoms showed any significant relationship with the neurological signs. The individual symptoms were then evaluated in relation to the urodynamic findings (Table 3). Eighty percent of the patients with detrusor hyperactivity complained of urgency, incontinence, or nocturnal incontinence, while 83.3% of the patients with sphincter disturbances had urine retention.
Distribution of Lower Urinary Tract Function by Neurological Deficits
Function
Group 1
Group 2
Group 3
Group 4
Number in each group Asymptomatic Asymptomatic and normal function Asymptomatic but abnormal function Symptomatic and abnormal function Total urodynamic abnormalities
8 8 (100) a 8 (100)
12 0 0
28 8 (28,6) 0
22 2 (9.1) 0
0
0
8
2
0
12 (100)
20 (71.4)
20 (90,9)
0
12 (100)
28 (100)
22 (100)
~Figures within parentheses represent percentages in each group
Urodynamic Findings with Spinal Lesions
Surg Neurol 1984;21:148-54
!
151
CERVICAL
14 ."-
DORSAL
13--
CONUS
12--
CAUDA EQUINA
tl-% Z M
10--
<
9-8--
O 7-7~ Z
6-5-4~ 3~ 2~
INCONTINENCE
URGENCY
HESITANCY
1. Distribution of patients according to symptoms of lower urinary tract dysfunction and site of lesion. Number of patients with incontinence and nocturnal incontinence is significantly higher among those with conus lesions. Figure
Incontinence was the most c o m m o n manifestation of urinary tract dysfunction, being seen in 2 5 . 7 % of the patients in the study population. O f the 18 patients who were incontinent, 12 (66%) had conus lesions, as compared to two (11%) with lesions at each of the other sites. Bladder sensation was reduced in 77.7% of the incontinent patients, while 8 8 . 8 % had a hyperactive detrusor. In 3 3 % of the patients, the cause of incontinence was detrusor hyperactivity with no sphincter disturbance. In 55% there was detrusor hyperactivity with sphincter abnormalities, and in the remaining 12% there was urethral incompetence. Thus, detrusor hyperactivity with or without sphincter disturbance was responsible for incontinence in 8 8 % of the patients, and urethral incompetence was responsible for incontinence in the remainder. Urgency was seen in 2 1 . 4 % of the patients, and was most evident among those with cauda equina lesions (46%) and least evident among those with dorsal lesions (13%); however, the difference was not statistically significant. All o f the patients with urgency had abnormal
RETENTION
NOCTURNAL INCONTINENCE
F'I~ E Q U E N ( Y
detrusor function with respect to contractility, sensation, or compliance. T h e r e was no relationship between urgency and any of the signs of neurological dysfunction in the study population. The urgency was caused by detrusor hyperreflexia and increased bladder sensation. Hesitancy and a p o o r urine stream were seen in 21% of the patients, being most c o m m o n among those with cauda equina lesions (46%) and equally distributed among those with lesions at other sites (13%). The cause of the hesitancy could generally be identified as either detrusor hypoactivity (areflexia, or noncontractility) causing an insufficient force of expulsion, or overactivity of the urethral sphincter (including dyssynergia), causing obstruction; however, there were nine patients with detrusor hyperreflexia and only seven with urethral overactivity or dyssynergia. Thus, the association of detrusor hyperactivity with hesitancy to two patients was difficult to explain. Urinary retention was seen in 17% of our entire patient group, but was not related to the site of the lesion in any of the affected patients. Bladder sensation was reduced in 6 6 % of the patients exhibiting retention. Detrusor contractility was normal in 4 1 % and compliance was normal in all but one. T h e urethra was overactive in 58% and dyssynergic in 25%. Thus, in 8 3 % of the patients with retention, the latter was due to urethral abnormalities causing obstruction, while detru-
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Gunasekera et al
Table 3. Analysis of Urodynamic Features with Type of the Symptom Function
Incontinence
Urgency
Hesitancy
Retention
Nocturnal incontinence
Frequency
N u m b e r in each g r o u p Site o f lesion U M N Cervical Dorsal LMN Conus Cauda equina Neurological deficits Group 1 Group 2 Group 3 Group 4 Bladder sensation Normal Reduced Increased Bladder compliance Normal Reduced Contractility Normal Hyperreflexic Areflexic Noncontractile Capacity Normal Reduced Increased Residual urine Positive Negative Urethra Normal Overactive Incompetent Dyssynergic N o r m a l bladder and abnormal sphincter Abnormal bladder and normal sphincter Abnormal sphincter and bladder
18
15
15
12
12
l1
2 2 12 2
3 2 4 6
3 3 3 6
3 4 2 3
2 0 7 3
3 0 3 5
0 5 4 9
0 2 5 8
0 4 5 6
0 2 7 3
0 5 2 5
0 1 4 6
3 14 1
3 9 3
4 10 1
3 8 1
3 7 2
2 7 2
8 10
10 5
11 4
11 1
2 10
6 5
0 16 2 0
2 10 0 3
2 9 3 1
5 3 1 3
0 10 1 1
2 2 0
8 9 1
8 3 4
12 1 2
9 1 2
9 3 0
5 4 2
16 2
10 5
8 7
9 3
7 4
6 5 3 4 0
9 1 1 4 0
7 3 1 4 2
2 7 0 3 5
6 1 1 4 0
5 1 1 4 1
6
9
8
2
6
5
12
6
5
5
6
5
sor areflexia or noncontractility was responsible for the retention in the remaining 17%. Nocturnal incontinence was seen in 17% of the patients, and was most c o m m o n in those with lower m o t o r neuron lesions (83%). D e t r u s o r compliance was reduced in a significantly higher proportion of patients with nocturnal incontinence as compared to those with other symptoms (p = 0.005); the contractility was abnormal in all patients with nocturnal incontinence, and 7 5 % had residual urine. T h e nocturnal incontinence was associated with detrusor hyperactivity (83%), reduced bladder compliance (83%), and residual urine in the bladder. In one patient this incontinence was associated with urethral incompetence.
---
Frequency of micturition was seen in 15.7% of the patients, and was m o r e evident in patients with lower m o t o r neuron lesions (73%) than in those with upper m o t o r neuron lesions (27%). In relation to the neurological deficits in the study population, frequency was most commonly seen in patients in groups 3 and 4, and was therefore m o r e associated with m o t o r deficits and sensory impairment than with sensory impairment alone. There was no relationship between frequency and any of the urodynamic findings. Postmicturition dribbling was seen in only one patient in the entire series. This patient had a cauda equina lesion and had detrusor sphincter dyssynergia with urethral instability, as shown by alternating contraction and
Urodynamic Findings with Spinal Lesions
relaxation of the urethral sphincter, which was probably responsible for the postmicturition dribble.
Discussion In this study there was a strong correlation between impaired pinprick sensation and lower urinary tract dysfunction. In the eight patients who had pyramidal weakness without impaired pinprick sensation, there was no disturbance of bladder or sphincter function, whereas all of the patients with sensory impairment had abnormal lower urinary tract function. Scott, in 1965, reported similar findings among 155 patients with lumbar disk protrusion, of whom 10 had symptoms of lower urinary tract dysfunction had impaired perianal sensation [ 11]. O'Laoire et al, in a 1981 study of recovery of sphincter function after surgery for lumbar disk protrusion, showed the significance of cutaneous sensations in relation to lower urinary tract function, pointing out that patients with persistent perianal hypoesthesia had persistent disturbances in urinary tract function [9]. Thus, the pathways subserving lower urinary tract function are likely to be very closely associated with the spinothalamic tract. Nathan and Smith, in 1951, studied the bladder function of patients with terminal malignant diseases who had had spinothalamic tractotomies for pain, and correlated the findings with the results of histologic studies of tract degeneration in the spinal cord obtained after the patients died [7]. They concluded that the centripetal pathways subserving bladder function are located in the equatorial plane of the spinal cord, very close to the spinothalamic tracts. A more recent study by Hitchcock et al of bladder function in patients who had had unilateral and bilateral spinothalamic tractotomies revealed similar findings [3]. In 1958, Nathan and Smith showed that the centrifugal pathways of bladder control are also located in a transverse bands across the width of the spinal cord [8]. In elaborate animal experiments, in which they used stimulation with micro-electrodes and focal destruction of the relevant pathways that control bladder function in cats, Kuru et al showed that subsequent tract degeneration, which outlined the descending pathways, occurred in the rubrospinal tracts ventral to and apart from the pyramidal tracts [5]. Some of the fibers were found to descend in the lateral columns to the intermediolateral nucleus of the sacral cord, which is the motor component of the sacral micturition center, while the remaining fibers were found to gradually shift anteriorly to descend in the anterior columns to the anterior horn cells of the sacral cord, which are the sacral neurons to the external sphincter. Kuru et al concluded that the pyramidal tracts were unlikely to play any part in the control of the lower urinary tract. Thus,
Surg Neurol 1984;21:148-54
153
our finding of a strong association of disturbed pinprick sensation with lower urinary tract function accords with the observations of others. There was a tendency for the incidence of lower urinary tract disturbance to increase with a descending lesion level on the spinal axis. The 100% incidence of clinically evident bladder disturbance with lesions of the cauda equina is probably exaggerated, since there was a tendency in this particular group to select, for urodynamic study, those patients with cauda equina lesions who had overt bladder disturbances. However, the finding of urodynamic abnormalities in 100~ of these patients accords with the observations of Konturi et al who, in a series of patients with lumbar disk herniations, found that all of 42 patients with prolapsed lumbar intervertebral disks had urodynamic abnormalities. Our finding also correlates with that of Rosomoff et al, who found that 8 3 ~ of their patients with lumbar disk protrusions had lower urinary tract dysfunction [4,10]. Such a tendency for lower urinary tract dysfunction to occur increasingly frequently with lesions at lower levels on the spinal axis could be due to the abundant space available in the cervical spinal canal as compared with that available in the region of the conus, with the result that a lesion in the cervical region would cause less pressure on the cord than a lesion in the conus region. Also, some of the tracts subserving bladder function are discrete in the cervical region while tending to merge further down the cord, with the effect that a lesion at a lower level has a greater possibility of causing bladder disturbance [6]. In 1967, Campbell showed that among 50 patients with spinal cord tumors, only 10 had symptoms of urinary disturbance, whereas all manifested urodynamic abnormalities [2]. We found asymptomatic urinary tract dysfunction in 14% of our patients with lower cord lesions and in 20% of those with upper motor neuron lesions. Clearly, urodynamic studies are essential for demonstrating lower tract dysfunction in asymptomatic patients. Incontinence was more common in patients with conus lesions, and urgency and hesitancy were seen with a slightly greater frequency in patients with cauda equina lesions than in those with other lesions; however, frequency and urinary retention showed no association with the site of the lesion in any of our patients. This contrasts with the observation of Campbell that patients with upper motor neuron lesions had frequency, urgency, and incontinence, while those with lower motor neuron lesions had hesitancy, a poor urine stream, and retention [2]. However, in our series, symptoms of obstruction could be attributed to abnormalities of urethral function, while symptoms associated with urine expulsion related more closely to detrusor dysfunction.
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Surg N e u r o l 1984;21:148-54
It is evident that in this series of 70 patients the urodynamic findings could, in most instances, explain the various symptoms observed in terms of abnormalities in detrusor or urethral function. Consequently, the importance of evaluating both of these functions in patients with neurogenic disturbances of the lower urinary tract cannot be overemphasized. We wish to thank the Nuffield Foundation for providing a traveling fellowship to permit this study to be conducted in London, the National Science Council of Sri Lanka for a grant, Mr. David Uttley and Mr. S. O'Laoire for allowing us to study their patients, Mr. M. Torrens for his valuable advice, Mr. R. Howard for his technical assistance, and Mrs. I. Van der Vord for secretarial service.
References 1. Bates CP, Bradley WE, Glen ES et al. Fourth report on the standardisation of terminology of lower urinary tract function. Br J Urol 1981;53:333-5. 2. Campbell EW. Bladder dysfunction related to lesions of the spinal cord. South Med J 1967;60:364-6.
G u n a s e k e r a et al
3. Hitchcock E, Newsome D, Salime M. The somatotopic representation of the micturition pathways in the cervical cord in man. B r J Surg 1974;61:395-401. 4. Konturi M, Harviainen S, Larmi TKT. Atonic bladder in lumbar disc herniation. Acta Chir Scand (Suppl) 1965;357:232-5. 5. Kuru M, Kurati T, Koyama Y. The bulbar vesical constrictor centre and the bulbo-sacral connections arising from it. A study of the functions of the lateral reticulo-spinal tract. J Comp Neurol 1959;113:365-88. 6. Kuru M. Nervous 1965;45:425-94.
control
of micturition.
Physiol
Rev
7. Nathan PW, Smith MC. The centripetal pathways from the bladder and urethra within the spinal cord. J Neurol Neurosurg Psychiatry 1951 ; 14:262-80. 8. Nathan PW, Smith MC. The centrifugal pathways for micturition within the spinal cord. J Neurol Neurosurg Psychiatry 1958;21:177-89. 9. O'Laoire SA, Crockard HA, Thomas DG. Prognosis for sphincter recovery after operation for cauda equina compression owing to lumbar disc prolapse. Br Med J 282:1852-4 10. Rosomoff HL, Johnston JDH, Gallo AE, et al. Cystometry as an adjunct in the evaluation of lumbar disc syndromes. J Neurosurg 1971;33:67-74. 11. Scott PJ. Bladder paralysis from cau~Ja equina lesions from disc prolapse. J Bone Joint Surg (Br) 1965;47B:224-35.
Surg Neurol 1984;21:148-54
Clinical Correlation of Urodynamic Findings in Patients with Localized Partial Lesions of the Spinal Cord and Cauda Equina W . S. L. G u n a s e k e r a , I. D . E v e r s d e n ,
F . R . C . S . , A. E. R i c h a r d s o n ,
F.R.C.S., K. N. Senevirame,
Ph.D.,
and
M.Phil.
Departments of Neurosurgery and Physiology, Atkinson Morley's Hospital, London, England
Gunasekera WSL, Richardson AE, Senevirame KN, Eversden ID. Clinical correlation of urodynamic findings in patients with localized partial lesions of the spinal cord and cauda equina. Surg Neurol 1984;21:148-54. Urodynamic studies were undertaken in 70 patients with incomplete, confirmed, localized lesions involving the spinal cord and cauda equina, irrespective of clinically evident bladder disturbances. Both detrusor and urethral function were simultaneously evaluated and correlated with neurological deficits and symptoms of lower urinary tract dysfunction. It was evident that in those patients with localized spinal cord lesions, lower urinary tract disturbances were closely associated with disturbances of pinprick sensation. Clinically silent bladder and sphincter dysfunction was encountered in 14% of the patients, and the number of asymptomatic patients was significantly higher among those with upper motor neuron lesions. Incontinence was associated predominantly with conus lesions; however, the other symptoms had no relationship to the site of the lesion. Symptoms such as urgency, incontinence, and nocturnal incontinence were associated with detrusor hyperactivity, and urinary retention was associated with urethral overactivity and dyssynergia. The urodynamic findings could explain the pathogenesis of the symptoms in most instances, but were not necessarily related to them. It is concluded that the pathways subserving lower-urinary-tract function are closely associated with the pathways subserving pinprick sensation, and that a lesion along the spinal axis can affect the bladder, sphincter, or both in a variety of ways, thus leading to the widely variable clinical findings associated with neurogenic lower urinary tract dysfunction. KEYWORDS: Spinal cord; Localized partial lesions; Neurogenic bladder; Neurological deficits; Urinary symptoms; Urodynamic studies; Cauda equina
Address reprint requests to." Mr. A.E. Richardson, F.R.C.S., Consultant Neurosurgeon, Atkinson Morley's Hospital, 31 Copse Hill, Wimbledon, London S.W. ZO ONE, England. Dr. Gunasekera's present address is: Neurosurgical Unit, General Hospital, Kandy, Sri Lanka. Dr. Senevirame's present address is: Department of Physiology, Faculty of Medicine, Colombo, Sri Lanka.
© 1984 by ElsevierSciencePublishingCo., Inc.
The urodynamic assessment o f patients with neurogenic bladder disturbances has led to a better understanding of the pathophysiology o f the lower urinary tract, as well as contributing to patient management. Urodynamic studies have also been helpful in demonstrating such problems in patients with neurological disease who have otherwise had no symptomatic evidence o f such disturbances. R o s o m o f f et al found that among 100 consecutive cases of confirmed lumbar disk protrusion, only 13% had symptoms of lower urinary tract dysfunction, whereas 8 3 % had abnormalities demonstrated by urodynamic assessment [10]. The aim of this study was to evaluate lower-urinarytract function in patients with commonly occurring, localized partial lesions of the spinal cord and cauda equina, and to correlate the urodynamic findings with the clinical manifestations in this population.
Material and Methods Seventy patients with localized lesions o f the spinal cord and cauda equina, demonstrated by myelography and subsequently confirmed at operation, were studied. There were 52 males and 18 females aged from 1 9 - 7 6 years, with a mean age of 43.1 years. T h e pathology of the lesions in this group included cervical spondylosis with posterior osteophytes, spinal-cord injuries, extra- and intradural tumors, prolapsed intervertebral disks, arteriovenous malformations of the spinal cord, and spina bifida with lipomas of the conus or diastomatomyelia. The patients were clinically evaluated* in relation to any urologic disturbances and neurological manifestations, and urodynamic studies were done on all of those with myelographically demonstrable lesions, irrespective of their urologic symptoms. Prior to urodynamic study, the patients were requested to e m p t y their blad-
*Methods, definitions, and units conform to the standards recommended by the International Continence Society, except where specifically mentioned. 0090-3019/84/$3.00
Urodynamic Findings with Spinal Lesions
ders. D e t r u s o r function was evaluated by cystometry with the patient in the supine position, using sterile normal saline at r o o m temperature, infused at a constant rate of 15 mL/min via a periurethral flexible nylon catheter of 1.0 m m external diameter (Portex, Ltd.), using a p u m p to maintain the necessary pressure head. T h e intravesical pressure was recorded via another, similar catheter lying alongside the first and connected to an external pressure transducer (Statham P 37). The intraabdominal pressure was simultaneously recorded via a fluid-filled rectal catheter, and this pressure was electronically subtracted from the intravesical pressure to indicate the detrusor pressure. T h e infusion was continued until patient tolerance was reached or until leakage occurred. T h e patients were then requested to void in the supine or seated position with the catheters in situ, in order to obtain a voiding cystometrogram. Any remaining fluid was evacuated and the residual urine volume was calculated by subtracting the voided and evacuated volumes from the volume infused. Urethral function was assessed by electromyographic studies of the perianal muscles using a percutaneous coaxial needle electrode inserted anterior to the anal orifice. The intravesical pressure, the intraabdominal pressure, the detrusor pressure, and the electromyogram were simultaneously recorded during filling and voiding, using a multichannel recorder. N o complications resulted from any of these procedures. From these measurements it was possible to evaluate bladder sensation, bladder compliance, detrusor contractility, the m a x i m u m cystometric capacity, the volume of residual urine, and urethral function. Bladder sensation was assessed subjectively, guided by the infusion volume at which the first desire to void was felt, and was considered normal if the desire to void appeared when the volume infused was between 100 mL and 300 mL; increased if the volume was less than 100 mL; and reduced if the volume was over 300 mL. Patients who became incontinent without a desire to void before 300 mL had been infused were also considered as having reduced sensation. Bladder compliance, C, was measured as the change of volume, AV, per unit increase in detrusor pressure, P, during filling (i.e., C = V/P). In a normal bladder, the capacity of which is usually below 500 mL, the increase in detrusor pressure occurs between 5 and 15 c m H 2 0 at m a x i m u m cystometric capacity, and the compliance was therefore considered normal if this pressure increase occurred between 5 and 15 c m H 2 0 ; reduced if it occurred at a pressure above 15 c m H 2 0 ; and increased if it occurred at a pressure below 5 c m H 2 0 . Detrusor contractility was considered normal if no sudden increases in detrusor pressure occurred during filling, and increased pressure occurred only with vol-
Surg Neurol 1984;21:148-54
149
untarily initiated voiding. If sudden increases in detrusor pressure occurred that the patient was unable to suppress they were considered as representing hyperreflexic contractility. If no voiding-pressure increase occurred in a bladder which was also abnormal in sensation or compliance, the contractility was classified as areflexic, and if a patient with normal sensation or compliance failed to initiate voiding, the detrusor was classified as noncontractile. The maximum cystometric capacity that the patient would tolerate was classified as normal if the volume of saline infused was between 150 and 500 mL; reduced if the volume was below 150 mL; and increased if the volume was over 500 mL. A residual urine volume of 10% greater than the maximum cystometric capacity was considered significant, and a volume below this value was considered as nonsignificant. The urethra was classified as normal or overactive according to the change in amplitude on the electromyogram during filling; dyssynergic if increased electromyographic activity occurred during attempted voiding; and incompetent if fluid leakage occurred without any increase in detrusor pressure. The symptoms of lower urinary tract dysfunction, and the urodynamic findings in each case, were then analyzed in relation to the site of the lesion and the neurological deficits.
Results There were 19 patients with cervical lesions, 15 with dorsal lesions, 23 with conus lesions, and 13 with cauda equina lesions. Lesions between D-10 and L-2 were classified as conus lesions. Patients with cervical and dorsal lesions had neurological signs of u p p e r m o t o r neuron dysfunction while those with conus and cauda equina lesions had signs of lower m o t o r neuron disturbance. There was a tendency for the proportion of patients with lower urinary tract dysfunction to increase as the site of the lesion descended, with the incidence of such dysfunction increasing from 4 7 . 4 % in patients with cervical lesions to 100% in those with cauda equina lesions (Table 1); however, this last figure may be an exaggeration, as there was an unintentional tendency to undertake urodynamic studies on patients with symptomatic bladder dysfunction in this particular group. Urodynamic assessment revealed that about half of the asymptomatic patients had abnormal lower urinary tract function. Abnormal urodynamic function was found in all of the patients with lower m o t o r neuron lesions, as compared to 76.4% of those with upper m o t o r neuron lesions; however, the difference was not statistically significant. T h e r e were eight patients with u p p e r m o t o r neuron lesions who had normal bladder and sphincter
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Gunasekera et al
Table 1. Distribution of Lower Urinary Tract Function by Site of the Lesion Lower motor neuron
Upper motor neuron
Function
Cervical
Dorsal
Total in each group Asymptomatic Asymptomatic and normal function Asymptomatic but abnormal function Symptomatic and abnormal function Total urodynamic abnormalities
19 10 (52.6) a 6
15 5 (33.3) 2
4
Conus
Cauda equina
23 3 (13) 0
3
3
Total
13 0 0
70 18 (25.7) 8 (11.4)
0
10 14.2)
9 (47.4)
10 (66.6)
20 (87)
13 (100)
52 (74.3)
13 (68.4)
13 (86.7)
23 (100)
13 (100)
62 (88.6)
~Figures within parentheses represent percentages in each group
function, whereas none of those with lower motor neuron lesions had normal lower urinary tract function. In order to evaluate the relationship between lower urinary tract function and signs of neurological dysfunction, the patients were divided into four groups. Group 1 comprised eight patients who had pyramidal weakness only, and no disturbance of pinprick sensation, while group 2 comprised 12 patients with impaired pinprick sensation only and no motor deficits. In group 3 there were 28 patients who had pyramidal weakness and impaired pinprick sensation below the level of the lesion, and in group 4 there were 22 patients who had segmental weakness and impaired pinprick sensation. None of the patients in group 1 had any symptoms of lower urinary tract dysfunction, while all of those in group 2 had such symptoms (Table 2). The symptoms were most frequent among those with sensory loss only (100%), and least frequent among those with pyramidal weakness and sensory impairment (71.4%). Upon urodynamic assessment, all of the patients in group 1 were found to have normal lower urinary tract function, while all of those in groups 2, 3, and 4 had
T a b l e 2.
abnormal function. Thus, all of those with normal pinprick sensation had normal lower urinary tract function, whereas all of those with impaired pinprick sensation had abnormal lower urinary tract function. The sensory impairment in the patients with abnormal lower urinary tract function was not limited to the sacral dermatomes, extending--in some patients--to a level in the trunk corresponding to the level of the lesion. The various symptoms of lower urinary tract function were next analyzed in relation to the site of the lesion (Figure 1). Incontinence and nocturnal incontinence were seen in significantly higher proportions in patients with conus lesions (p = < 0.005), but there was no relationship between any of the other symptoms and the site of the lesion. None of the symptoms showed any significant relationship with the neurological signs. The individual symptoms were then evaluated in relation to the urodynamic findings (Table 3). Eighty percent of the patients with detrusor hyperactivity complained of urgency, incontinence, or nocturnal incontinence, while 83.3% of the patients with sphincter disturbances had urine retention.
Distribution of Lower Urinary Tract Function by Neurological Deficits
Function
Group 1
Group 2
Group 3
Group 4
Number in each group Asymptomatic Asymptomatic and normal function Asymptomatic but abnormal function Symptomatic and abnormal function Total urodynamic abnormalities
8 8 (100) a 8 (100)
12 0 0
28 8 (28,6) 0
22 2 (9.1) 0
0
0
8
2
0
12 (100)
20 (71.4)
20 (90,9)
0
12 (100)
28 (100)
22 (100)
~Figures within parentheses represent percentages in each group
Urodynamic Findings with Spinal Lesions
Surg Neurol 1984;21:148-54
!
151
CERVICAL
14 ."-
DORSAL
13--
CONUS
12--
CAUDA EQUINA
tl-% Z M
10--
<
9-8--
O 7-7~ Z
6-5-4~ 3~ 2~
INCONTINENCE
URGENCY
HESITANCY
1. Distribution of patients according to symptoms of lower urinary tract dysfunction and site of lesion. Number of patients with incontinence and nocturnal incontinence is significantly higher among those with conus lesions. Figure
Incontinence was the most c o m m o n manifestation of urinary tract dysfunction, being seen in 2 5 . 7 % of the patients in the study population. O f the 18 patients who were incontinent, 12 (66%) had conus lesions, as compared to two (11%) with lesions at each of the other sites. Bladder sensation was reduced in 77.7% of the incontinent patients, while 8 8 . 8 % had a hyperactive detrusor. In 3 3 % of the patients, the cause of incontinence was detrusor hyperactivity with no sphincter disturbance. In 55% there was detrusor hyperactivity with sphincter abnormalities, and in the remaining 12% there was urethral incompetence. Thus, detrusor hyperactivity with or without sphincter disturbance was responsible for incontinence in 8 8 % of the patients, and urethral incompetence was responsible for incontinence in the remainder. Urgency was seen in 2 1 . 4 % of the patients, and was most evident among those with cauda equina lesions (46%) and least evident among those with dorsal lesions (13%); however, the difference was not statistically significant. All o f the patients with urgency had abnormal
RETENTION
NOCTURNAL INCONTINENCE
F'I~ E Q U E N ( Y
detrusor function with respect to contractility, sensation, or compliance. T h e r e was no relationship between urgency and any of the signs of neurological dysfunction in the study population. The urgency was caused by detrusor hyperreflexia and increased bladder sensation. Hesitancy and a p o o r urine stream were seen in 21% of the patients, being most c o m m o n among those with cauda equina lesions (46%) and equally distributed among those with lesions at other sites (13%). The cause of the hesitancy could generally be identified as either detrusor hypoactivity (areflexia, or noncontractility) causing an insufficient force of expulsion, or overactivity of the urethral sphincter (including dyssynergia), causing obstruction; however, there were nine patients with detrusor hyperreflexia and only seven with urethral overactivity or dyssynergia. Thus, the association of detrusor hyperactivity with hesitancy to two patients was difficult to explain. Urinary retention was seen in 17% of our entire patient group, but was not related to the site of the lesion in any of the affected patients. Bladder sensation was reduced in 6 6 % of the patients exhibiting retention. Detrusor contractility was normal in 4 1 % and compliance was normal in all but one. T h e urethra was overactive in 58% and dyssynergic in 25%. Thus, in 8 3 % of the patients with retention, the latter was due to urethral abnormalities causing obstruction, while detru-
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Table 3. Analysis of Urodynamic Features with Type of the Symptom Function
Incontinence
Urgency
Hesitancy
Retention
Nocturnal incontinence
Frequency
N u m b e r in each g r o u p Site o f lesion U M N Cervical Dorsal LMN Conus Cauda equina Neurological deficits Group 1 Group 2 Group 3 Group 4 Bladder sensation Normal Reduced Increased Bladder compliance Normal Reduced Contractility Normal Hyperreflexic Areflexic Noncontractile Capacity Normal Reduced Increased Residual urine Positive Negative Urethra Normal Overactive Incompetent Dyssynergic N o r m a l bladder and abnormal sphincter Abnormal bladder and normal sphincter Abnormal sphincter and bladder
18
15
15
12
12
l1
2 2 12 2
3 2 4 6
3 3 3 6
3 4 2 3
2 0 7 3
3 0 3 5
0 5 4 9
0 2 5 8
0 4 5 6
0 2 7 3
0 5 2 5
0 1 4 6
3 14 1
3 9 3
4 10 1
3 8 1
3 7 2
2 7 2
8 10
10 5
11 4
11 1
2 10
6 5
0 16 2 0
2 10 0 3
2 9 3 1
5 3 1 3
0 10 1 1
2 2 0
8 9 1
8 3 4
12 1 2
9 1 2
9 3 0
5 4 2
16 2
10 5
8 7
9 3
7 4
6 5 3 4 0
9 1 1 4 0
7 3 1 4 2
2 7 0 3 5
6 1 1 4 0
5 1 1 4 1
6
9
8
2
6
5
12
6
5
5
6
5
sor areflexia or noncontractility was responsible for the retention in the remaining 17%. Nocturnal incontinence was seen in 17% of the patients, and was most c o m m o n in those with lower m o t o r neuron lesions (83%). D e t r u s o r compliance was reduced in a significantly higher proportion of patients with nocturnal incontinence as compared to those with other symptoms (p = 0.005); the contractility was abnormal in all patients with nocturnal incontinence, and 7 5 % had residual urine. T h e nocturnal incontinence was associated with detrusor hyperactivity (83%), reduced bladder compliance (83%), and residual urine in the bladder. In one patient this incontinence was associated with urethral incompetence.
---
Frequency of micturition was seen in 15.7% of the patients, and was m o r e evident in patients with lower m o t o r neuron lesions (73%) than in those with upper m o t o r neuron lesions (27%). In relation to the neurological deficits in the study population, frequency was most commonly seen in patients in groups 3 and 4, and was therefore m o r e associated with m o t o r deficits and sensory impairment than with sensory impairment alone. There was no relationship between frequency and any of the urodynamic findings. Postmicturition dribbling was seen in only one patient in the entire series. This patient had a cauda equina lesion and had detrusor sphincter dyssynergia with urethral instability, as shown by alternating contraction and
Urodynamic Findings with Spinal Lesions
relaxation of the urethral sphincter, which was probably responsible for the postmicturition dribble.
Discussion In this study there was a strong correlation between impaired pinprick sensation and lower urinary tract dysfunction. In the eight patients who had pyramidal weakness without impaired pinprick sensation, there was no disturbance of bladder or sphincter function, whereas all of the patients with sensory impairment had abnormal lower urinary tract function. Scott, in 1965, reported similar findings among 155 patients with lumbar disk protrusion, of whom 10 had symptoms of lower urinary tract dysfunction had impaired perianal sensation [ 11]. O'Laoire et al, in a 1981 study of recovery of sphincter function after surgery for lumbar disk protrusion, showed the significance of cutaneous sensations in relation to lower urinary tract function, pointing out that patients with persistent perianal hypoesthesia had persistent disturbances in urinary tract function [9]. Thus, the pathways subserving lower urinary tract function are likely to be very closely associated with the spinothalamic tract. Nathan and Smith, in 1951, studied the bladder function of patients with terminal malignant diseases who had had spinothalamic tractotomies for pain, and correlated the findings with the results of histologic studies of tract degeneration in the spinal cord obtained after the patients died [7]. They concluded that the centripetal pathways subserving bladder function are located in the equatorial plane of the spinal cord, very close to the spinothalamic tracts. A more recent study by Hitchcock et al of bladder function in patients who had had unilateral and bilateral spinothalamic tractotomies revealed similar findings [3]. In 1958, Nathan and Smith showed that the centrifugal pathways of bladder control are also located in a transverse bands across the width of the spinal cord [8]. In elaborate animal experiments, in which they used stimulation with micro-electrodes and focal destruction of the relevant pathways that control bladder function in cats, Kuru et al showed that subsequent tract degeneration, which outlined the descending pathways, occurred in the rubrospinal tracts ventral to and apart from the pyramidal tracts [5]. Some of the fibers were found to descend in the lateral columns to the intermediolateral nucleus of the sacral cord, which is the motor component of the sacral micturition center, while the remaining fibers were found to gradually shift anteriorly to descend in the anterior columns to the anterior horn cells of the sacral cord, which are the sacral neurons to the external sphincter. Kuru et al concluded that the pyramidal tracts were unlikely to play any part in the control of the lower urinary tract. Thus,
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153
our finding of a strong association of disturbed pinprick sensation with lower urinary tract function accords with the observations of others. There was a tendency for the incidence of lower urinary tract disturbance to increase with a descending lesion level on the spinal axis. The 100% incidence of clinically evident bladder disturbance with lesions of the cauda equina is probably exaggerated, since there was a tendency in this particular group to select, for urodynamic study, those patients with cauda equina lesions who had overt bladder disturbances. However, the finding of urodynamic abnormalities in 100~ of these patients accords with the observations of Konturi et al who, in a series of patients with lumbar disk herniations, found that all of 42 patients with prolapsed lumbar intervertebral disks had urodynamic abnormalities. Our finding also correlates with that of Rosomoff et al, who found that 8 3 ~ of their patients with lumbar disk protrusions had lower urinary tract dysfunction [4,10]. Such a tendency for lower urinary tract dysfunction to occur increasingly frequently with lesions at lower levels on the spinal axis could be due to the abundant space available in the cervical spinal canal as compared with that available in the region of the conus, with the result that a lesion in the cervical region would cause less pressure on the cord than a lesion in the conus region. Also, some of the tracts subserving bladder function are discrete in the cervical region while tending to merge further down the cord, with the effect that a lesion at a lower level has a greater possibility of causing bladder disturbance [6]. In 1967, Campbell showed that among 50 patients with spinal cord tumors, only 10 had symptoms of urinary disturbance, whereas all manifested urodynamic abnormalities [2]. We found asymptomatic urinary tract dysfunction in 14% of our patients with lower cord lesions and in 20% of those with upper motor neuron lesions. Clearly, urodynamic studies are essential for demonstrating lower tract dysfunction in asymptomatic patients. Incontinence was more common in patients with conus lesions, and urgency and hesitancy were seen with a slightly greater frequency in patients with cauda equina lesions than in those with other lesions; however, frequency and urinary retention showed no association with the site of the lesion in any of our patients. This contrasts with the observation of Campbell that patients with upper motor neuron lesions had frequency, urgency, and incontinence, while those with lower motor neuron lesions had hesitancy, a poor urine stream, and retention [2]. However, in our series, symptoms of obstruction could be attributed to abnormalities of urethral function, while symptoms associated with urine expulsion related more closely to detrusor dysfunction.
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It is evident that in this series of 70 patients the urodynamic findings could, in most instances, explain the various symptoms observed in terms of abnormalities in detrusor or urethral function. Consequently, the importance of evaluating both of these functions in patients with neurogenic disturbances of the lower urinary tract cannot be overemphasized. We wish to thank the Nuffield Foundation for providing a traveling fellowship to permit this study to be conducted in London, the National Science Council of Sri Lanka for a grant, Mr. David Uttley and Mr. S. O'Laoire for allowing us to study their patients, Mr. M. Torrens for his valuable advice, Mr. R. Howard for his technical assistance, and Mrs. I. Van der Vord for secretarial service.
References 1. Bates CP, Bradley WE, Glen ES et al. Fourth report on the standardisation of terminology of lower urinary tract function. Br J Urol 1981;53:333-5. 2. Campbell EW. Bladder dysfunction related to lesions of the spinal cord. South Med J 1967;60:364-6.
G u n a s e k e r a et al
3. Hitchcock E, Newsome D, Salime M. The somatotopic representation of the micturition pathways in the cervical cord in man. B r J Surg 1974;61:395-401. 4. Konturi M, Harviainen S, Larmi TKT. Atonic bladder in lumbar disc herniation. Acta Chir Scand (Suppl) 1965;357:232-5. 5. Kuru M, Kurati T, Koyama Y. The bulbar vesical constrictor centre and the bulbo-sacral connections arising from it. A study of the functions of the lateral reticulo-spinal tract. J Comp Neurol 1959;113:365-88. 6. Kuru M. Nervous 1965;45:425-94.
control
of micturition.
Physiol
Rev
7. Nathan PW, Smith MC. The centripetal pathways from the bladder and urethra within the spinal cord. J Neurol Neurosurg Psychiatry 1951 ; 14:262-80. 8. Nathan PW, Smith MC. The centrifugal pathways for micturition within the spinal cord. J Neurol Neurosurg Psychiatry 1958;21:177-89. 9. O'Laoire SA, Crockard HA, Thomas DG. Prognosis for sphincter recovery after operation for cauda equina compression owing to lumbar disc prolapse. Br Med J 282:1852-4 10. Rosomoff HL, Johnston JDH, Gallo AE, et al. Cystometry as an adjunct in the evaluation of lumbar disc syndromes. J Neurosurg 1971;33:67-74. 11. Scott PJ. Bladder paralysis from cau~Ja equina lesions from disc prolapse. J Bone Joint Surg (Br) 1965;47B:224-35.