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Outcome in Patients Who Underwent Tethered Cord Release for Occult Spinal Dysraphism
Outcome in Patients Who Underwent Tethered Cord Release for Occult Spinal Dysraphism Luis Antonio Guerra,* John Pike,† Julie Milks, Nicholas Barrowman‡ and Michael Leonard† From the Division of Pediatric Urology and Chalmers Research Group-Research Institute (NB), Children’s Hospital of Eastern Ontario, University of Ottawa, Ottawa, Ontario, Canada
Purpose: Tethered cord syndrome encompasses a group of clinical symptoms caused by abnormal spinal cord fixation. We evaluated a select cohort of patients with primary tethered cord syndrome in regard to urodynamic and clinical outcome after cord release. Materials and Methods: We retrospectively reviewed the records of patients with the diagnosis of tethered cord from May 2001 to October 2004. Patients were assessed preoperatively by standard urodynamic studies, which was repeated a mean of 6.4 months after tethered cord release. Clinical and urodynamic outcomes were analyzed. Results: Ten male and 14 female patients 1 month to 12 years old (median age 6 years) were evaluable. Preoperatively 14 of the 24 patients with a median age of 8.1 years were toilet trained and 7 (50%) had diurnal incontinence. Constipation was noted in 10 of 24 patients (42%) and urinary tract infections developed in 6 (25%). Postoperatively only 1 patient (7%) experienced diurnal incontinence (p ⫽ 0.04). Constipation was observed in 6 patients (25%) and urinary tract infections developed in 1 (4.2%) (p ⫽ 0.29 and 0.07, respectively). Ten of the 21 children (48%) with abnormal urodynamics had normalized studies postoperatively. Ten of the 17 patients with neurogenic detrusor overactivity achieved normalization and 7 remained unchanged. Two of 3 patients with normal preoperative urodynamics had neurogenic detrusor overactivity and 1 had poor bladder compliance. Four patients with low bladder capacity and/or low compliance preoperatively did not improve. Conclusions: Our results suggest that tethered cord release is beneficial in terms of clinical and urodynamic outcomes. Patients with abnormal urodynamics had 48% improvement after tethered cord release. Neurogenic detrusor overactivity seems to respond better with 59% improvement in urodynamics. The level of the conus on magnetic resonance imaging did not seem to be predictive of urodynamic outcome. Patients with a normal bladder may show urodynamic deterioration postoperatively, which raises cause for concern. Key Words: spinal cord, urodynamics, neurogenic bladder, spinal dysraphism
ccult spinal dysraphism (primary TC) refers to a select group of spinal abnormalities associated with a posterior bony spinal defect that develops beneath an intact dermis and epidermis.1 It includes spinal and caudaequina lipoma, diastematomyelia, lipomyelomeningocele, dorsal dermal sinus, neural enteric cyst and filum terminale syndrome. Spinal cord tethering may also be secondary to surgery or infection. Developmental anomalies of the spinal cord often result in neurological bladder dysfunction. The most common and widely recognized of these anomalies is myelomeningocele, which is associated with neurogenic vesical dysfunction in more than 90% of patients.2 TC syndrome refers to a group of clinical symptoms caused by abnormal spinal cord fixation. When the spinal cord is tethered, there is a limitation of its motion, which may lead to ischemic damage of the
O
Study received Institutional Review Board approval. * Correspondence and requests for reprints: Department of Urology, Children’s Hospital of Eastern Ontario, 401 Smyth Rd., K1H 8L1, Ottawa, Ontario, Canada (e-mail: [email protected]). † Financial interest and/or other relationship with Q-Med Canada. ‡ Financial interest and/or other relationship with Canadian Medical Association and Medico-Legal Conference.
0022-5347/06/1764-1729/0 THE JOURNAL OF UROLOGY® Copyright © 2006 by AMERICAN UROLOGICAL ASSOCIATION
neural tissue secondary to neural root stretching. It is well documented that children may present with neurological, orthopedic, dermatological and urological manifestations of TC syndrome.3 Although some published series of TC release show contradictory results,4 many groups have documented the benefit of TC release in children with subsequent improvement in clinical and urodynamic parameters.2–5 Fone et al found surgery to be beneficial in a group with primary TC and no improvement when releasing secondary tethered cords.2 We evaluated a select group of patients with primary TC syndrome in regard to urodynamic and clinical outcomes.
MATERIALS AND METHODS We performed an Institutional Review Board approved, retrospective review of the records of patients with a clinical diagnosis of TC due to spinal dysraphism who were referred for urodynamic evaluation from May 2001 to October 2004. All patients underwent TC release, as performed by the neurosurgery team at our institution. The children were assessed preoperatively with UDS, which was repeated a mean of 6.4 months after TC release. Clinical and urodynamic outcomes were compared between the 2 periods. The diagnosis of TC was based on history and
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physical examination, and all children underwent spinal cord MRI. Complete urological evaluation was done, including ultrasound of the upper tract. Intraoperative urodynamics were used to guide the manipulation of nerve roots and avoid injury to the lower urinary tract innervation. Intravesical and intrarectal pressure were recorded using standard urodynamic equipment and pelvic floor muscle activity was monitored during surgery with electromyography and intrarectal electrodes. Clinical outcomes were evaluated for the last 6-month period preoperatively and for a mean followup of 6 months after surgery. Clinical outcomes were urinary and fecal incontinence, constipation, UTI, and the use of oxybutynin, antibiotic prophylaxis and CIC. UDS parameters evaluated were total bladder capacity, pressure at total bladder capacity, compliance, neurogenic detrusor overactivity, post-void residual urine volume and detrusor leak point pressure. Differences in dichotomous outcomes preoperatively vs postoperatively were assessed using the McNemar chisquare test with a continuity correction. The CI for these differences was calculated using the normal approximation with a continuity correction. RESULTS A total of 24 patients were included in this study, including 10 males and 14 females 1 month to 12 years old (median age 6 years). All patients were ambulatory and diagnosed with occult spinal dysraphism. Patients with TC and a history of spinal cord surgery, trauma or TC secondary to infectious conditions were excluded. Table 1 lists lower back findings, lower limb complaints and MRI findings in our patient population. Incontinence and UTI were the most common urinary symptoms, while constipation was the most frequent intestinal complaint. Table 2 shows clinical outcomes after surgery. Preoperatively 14 of 24 patients (58%) were toilet trained and they had a median age of 8.1 years (range 3 to 12), while 10 (42%) who were not toilet trained had a median age of 8 months (range 1 to 12). Seven of the 14 toilet trained patients (50%) had daytime incontinence associated with urgency and frequency preoperatively and only 1 (7%) remained incontinent after surgery. All 7 patients who were
TABLE 1. Patients with abnormal lower back examination, lower limb complaints and MRI findings No. Pts (%) Lower back examination: Skin dimple/gluteal cleft asymmetry Hemangioma ⫹ hair tuft Sacral fat pad Small meningocele (micro meningocele) Scoliosis Normal Lower limb complaints: Gait abnormality Pain Weakness/numbness 1 Leg smaller 1 Foot smaller None MRI findings: Thickened filum Lipoma Syrinx Spina bifida occulta Diastematomyelia (split cord malformation.)
24 9 (37) 5 (21) 3 (13) 2 (8) 2 (8) 3 (13) 4 (17) 3 (13) 2 (8) 2 (8) 2 (8) 11 (46) 9 (37) 9 (37) 8 (33) 5 (21) 4 (17)
TABLE 2. Preoperative and postoperative clinical and urodynamic parameters
No. clinical outcome/total No. (%): Daytime incontinence* Constipation UTI Oxybutinin CIC Urodynamic outcome: Mean bladder capacity ⫾ SD (ml) Mean bladder capacity pressure ⫾ SD (cm H2O) Mean compliance ⫾ SD (ml/cm H2O) No. neurogenic detrusor overactivity Mean ml post-void residual urine vol (% bladder vol)
Preop
Postop
7/14 (50) 10/24 (42) 6/24 (25) 2/24 (8) 2/24 (8)
1/14 (7) 6/24 (25) 1/24 (4) 2/24 (8) 3/24 (12)
103.9 ⫾ 68.2 36.2 ⫾ 28.6
148.6 ⫾ 89.7 17.2 ⫾ 25.4
5.8 ⫾ 5.2 17 19.6 (18.2)
23.6 ⫾ 19.9 11 4.7 (3.1)
* Assessed only in toilet trained patients (older than 3 years).
continent preoperatively remained continent following surgery. Thus, only 1 of the 14 patients (7.1%) was incontinent following surgery (p ⫽ 0.04). The change was – 42.9% (95% CI – 82.8% to –2.9%). In the total group constipation was present in 10 of 24 patients (42%) preoperatively, of whom only 4 continued to experience constipation following surgery. Two of the 14 patients who did not experience constipation preoperatively experienced constipation following surgery. Thus, 6 patients (25.0%) experienced constipation postoperatively (p ⫽ 0.29). The change was ⫺16.7% (95% CI – 46.9% to 13.6%). Preoperatively UTI was present in 6 of the 24 patients (25.0%) and following surgery only 1 of the 6 had UTI. None of the 18 patients who were free of UTI preoperatively had UTI following surgery. Thus, only 1 of the 24 patients (4.2%) had UTI following surgery (p ⫽ 0.07). The change was –20.8% (95% CI ⫺45.2% to 3.6%). None of the 24 patients had stool soiling. Two children were on oxybutynin and CIC. No patient was on antibiotic prophylaxis. The 2 patients on oxybutynin orally continued the drug postoperatively. Two patients on CIC preoperatively continued in the postoperative period and another was started on CIC due to a low compliant bladder. Table 2 lists preoperative and postoperative urodynamic parameter changes. UDS was performed an average of 6.4 months after TC release. There was no patient with an areflexic detrusor before or after surgery in our series. To facilitate analysis we grouped urodynamic patterns as hyperreflexic, low compliance/capacity and normal bladders. Of the 24 patients 17 had a hyperreflexic bladder, including 10 (59%) in whom the pattern normalized, 6 who remained unchanged and 1 in whom a low compliance bladder developed. Four of the 24 patients had low bladder capacity and/or compliance, and no improvement after TC release. Three of the 24 patients had normal preoperative UDS, of whom 2 had a hyperreflexic bladder and 1 had poor bladder compliance. Thus, overall 21 of the 24 patients (87.5%) had some UDS abnormality preoperatively compared to 14 (58.3%) postoperatively (p ⫽ 0.10). The change was ⫺29.2% (95% CI ⫺64.4% to 6.0%). Considering the outcome in these 21 patients who had UDS abnormality preoperatively 10 (48%) improved after TC release, of whom all had neurogenic detrusor overactivity. Of the 24 patients 17 (71%) had the conus medullaris at L3 or below, while 7 (29%) had the conus at L1 or L2. Of the
TETHERED CORD RELEASE FOR OCCULT SPINAL DYSRAPHISM 17 patients with neurogenic detrusor overactivity preoperatively 14 (82%) had the conus medullaris at or below L3 before surgery, while only 3 (18%) had the conus at L1-L2. Postoperatively 7 of the 10 patients (70%) with neurogenic detrusor overactivity in whom UDS normalized had the conus at L3 or below. Three patients had split cord malformation (diastematomyelia) and only 1 had a normalized UDS. Two patients presented with progressive and worsening scoliosis, and neither responded to TC release. When we stratified patients by age, there was no statistically significant difference in these clinical and urodynamic outcomes. DISCUSSION The lesions of neural tube defects are variations of the normal development of the spine and spinal cord. Knowledge of the normal embryology allows better understanding of these defects and the anatomical relationships seen on diagnostic studies.6 A number of pathological conditions have been described under the label of spinal dysraphism, including congenital anomalies of the caudal spinal cord and distal vertebral column. They do not result in an open vertebral canal. Because they are defects covered by skin and subcutaneous tissue, many groups refer to them as occult dysraphism. Classically the lower part of the conus medullaris should lie at L1-L2 and the normal filum terminale should be less than 2 mm wide at the L5-S1 level. There has been some discussion as to whether a normal level conus medullaris could be tethered without lying in a low position on MRI. Our series showed that 17 of 24 patients (71%) had a conus at L3 or below. Only 7 of these 17 patients (41%) with a low conus preoperatively had normal UDS postoperatively. Seven children had the conus at the normal L1-L2 level and 3 (42%) had a good response. Thus, the position of the conus alone was not a factor predictive of outcome in the entire patient cohort and some patients with a normal conus on MRI benefited from TC release. In TC syndrome the distal lumbar spinal cord is fixed at 2 points, that is 1 at the site of tethering and the other at the level of the exit of the nerve roots. During extension, flexion or the abdominal Valsalva maneuver there is a lack of motion and stretching of the cord and roots, which can lead to ischemia and an anaerobic metabolism.7 The clinical findings of TC result from the cumulative damage of intermittent neuronal hypoxemia.8,9 Because interneuronal axon connections require an aerobic metabolism, they are the first affected and clinically this leads to urinary incontinence and a decreased skeletal muscle reflex. In contrast, the long neuronal tracts involving muscular movement are less susceptible to hypoxic injury and, hence, the findings of lower limb weakness with associated hyperreflexia and an upward Babinski reflex are delayed manifestations of neurological impairment.8 UDS is can anticipate neurological bladder dysfunction secondary to TC and it is often done. Loss of the sacral reflex arc and the development of neurogenic detrusor overactivity are the earliest alterations that can be detected by physical and urodynamic examinations. In this study patients with neurogenic detrusor overactivity on preoperative UDS were the only ones who responded favorably to TC release. Of these 17 patients 14 (82%) had the conus at a low position at L3 or below. When we correlated neurogenic detrusor overactivity and the level of the conus with normal UDS postoperatively, there was a 50% response (7 of 14
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patients) for the conus at or below L3 and a 100% response (3 of 3) for the conus at L1 and L2. These findings may show that, although a lower conus is unquestionably pathological, patients with neurogenic detrusor overactivity and a normal level conus may also have a significant pathological condition and they may respond to TC release. This may suggest that such patients with a normal level conus have a less severe form of cord tethering with decreased end organ damage. The presence of syrinx, lipoma, diastematomyelia or thick filum on MRI were not predictive of postoperative outcome in this study. Newborns and infants evaluated for possible TC usually have a normal neurological examination. Urodynamic studies show an abnormality in approximately a third of infants and children younger than 18 months.10,11 Urinary symptoms do not seem to be consistently present but when they manifest they are usually secondary to neurogenic detrusor overactivity, leading to incontinence, urgency and urinary frequency. Less frequently one can detect detrusor sphincter dyssynergia on UDS. Palmer et al found occult changes in the bladder in 75% of children with myelodysplasia who did not have clinical manifestations of TC syndrome referable to the urinary tract.12 The indication for surgical treatment for TC is often a challenging decision. MRI and US are not completely reliable for assessing the filum terminale and currently to our knowledge there is no test to confirm metabolic suffering of the neuronal cell. It is still unclear if all children with neurological signs of TC experience deterioration if the cord is not untethered. The literature contains several small series of the pros and cons of surgery. To our knowledge there are no proven long-term data to predict which patient may benefit from the procedure or whether the unreleased cord would neurologically deteriorate with time. More worrisome is the fact that 10% of patients with a normal bladder have neurogenic bladder after surgical untethering.10 Unfortunately there is no strong evidence to answer these uncertainties. Most neurosurgeons rely on their clinical judgement and experience to decide whether to intervene. Daytime urinary incontinence is a bothersome symptom that impairs quality of life. In our series it was present in 50% of the children and it dramatically improved, decreasing to 7% after cord untethering. Neurogenic detrusor overactivity bladder had the highest response rate among urodynamic parameters with resolution in 59% of cases. Similar results were reported by Khoury et al in a group of 31 select children with TC who had occult dysraphism.5 They noted 72% improvement in urinary incontinence after releasing the cord and 59% resolution of neurogenic detrusor overactivity.5 Unlike the data reported by Flanigan13 and Kondo14 et al showing that 71% and 60% of patients with TC, respectively, had an acontractile detrusor, we had no patient with this bladder pattern in our study. There is great controversy about the most common pattern of UDS in TC and the result reported by Kondo et al was among in adult population. Detrusor-sphincter dyssynergia is not commonly described in these patients. Constipation is not frequently referred in the literature as associated with tethered cord. Rosen et al noted that only 9% of children with spinal cord abnormalities had intractable constipation but TC was the most common association.15 We found constipation in 42% of our patients, which decreased to 25% after surgery. A decrease in UTI from 25% to
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4% may have been related to a decrease in post-void residual urine from 18% to 3% of total bladder volume, which was associated with improvement in intestinal constipation or bladder function after TC release. Mean bladder capacity improved from 103.9 to 148.6 ml after surgery, representing a 43% increase in bladder storage volume. Similar improvement was observed in mean bladder compliance, which increased from 5.8 to 23.6 ml/cm H2O. Improved bladder compliance is the result of better vesical function after surgery and it may reflect reversibility of the neural lesion. Keating10 and Kondo14 et al reported better results when TC is identified and released early and they emphasized the necessity of correction before the lesion becomes permanent. In our series age at surgery was not predictive of a better outcome. Surgery to untether the spinal cord is not without risk. In fact, a 12% risk of deterioration was observed postoperatively in patients with normal preoperative UDS in 1 reported series.10 We observed a higher rate of bladder deterioration. Two of the 3 patients with a normal bladder on UDS preoperatively had neurogenic detrusor overactivity and 1 had a low compliance pattern on postoperative evaluation. In our series bladders with low capacity and low compliance did not benefit from surgery. We postulate that this may reflect a structural end stage organ lesion with collagen deposition in place of normal smooth muscle. If further studies confirm this finding, we should consider avoiding TC release in such children. Two patients with neurogenic detrusor overactivity, who were on CIC, and oral and intravesical oxybutynin preoperatively, continued with the same treatment after surgery. One child had an excellent response with bladder capacity increasing from 77 to 189 ml, although compliance increased less, that is from 12 to 17 ml/cm H2O. In the other child treatment failed with preoperative and postoperative compliance of 3 and 4.1 ml/cm H2O, respectively. A male patient with neurogenic detrusor overactivity and a compliance of 1.2 ml/cm H2O preoperatively began CIC after surgery but followup UDS showed a normal pattern with a compliance of 20 ml/cm H2O. Our study has limitations related to its retrospective analysis and inherent bias. There have been several reports of UDS parameters associated with neurological disease in the pediatric population.16 –19 However, the definition of normal UDS in a child who is not toilet trained is a challenging situation that may create definition bias in the results. Although our sample was small and we had limited power to detect changes, our results suggest that TC release is beneficial in terms of clinical and urodynamic outcomes. CONCLUSIONS Our results suggest that TC release is beneficial in terms of clinical and urodynamic outcomes. Patients with abnormal urodynamics had 48% improvement postoperatively. Children with neurogenic detrusor overactivity seem to respond better with 59% improvement in UDS. The level of the conus on MRI and age at intervention did not seem to be predictive of the urodynamic outcome. Low capacity/poorly compliant bladders did not benefit urodynamically from this intervention. Patients with a normal bladder may show urodynamic deterioration postoperatively, which raises cause for concern.
Abbreviations and Acronyms BC BV CIC MRI TC UDS US UTI
⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽
bladder capacity bladder volume clean intermittent catheterization magnetic resonance imaging tethered cord urodynamic study ultrasound urinary tract infection
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Husmann, D. A.: Occult spinal dysraphism (the tethered cord) and the urologist. AUA Update Series, XIV:lesson 10, p. 78, 1995 Patricia, D. F., Vapnek, J. M., Litwiller, S. E., Couillard, D. R., McDonald, C. M., Boggan, J. E. et al: Urodynamic findings in the tethered spinal cord syndrome: does surgical release improve bladder function? J Urol, 157: 604, 1997 Hoffman, H. J., Hendrick, E. B. and Humphreys, R. P.: The tethered spinal cord: its protean manifestations, diagnosis and surgical correction. Child Brain, 2: 145, 1976 Giddens, J. L., Radomski, S. B., Hirshberg, E. D., Hassouna, M. and Fehlings, M.: Urodynamic findings in adults with tethered cord syndrome. J Urol, 161: 1249, 1999 Khoury, A. E., Hendrick, E. B., McLorie, G. A., Kulkarni, A. and Churchill, B. M.: Occult spinal dysraphism: clinical and urodynamic outcome after division of the filum terminale. J Urol, 144: 426, 1990 Kaufman, B. A.: Neural tube defects. Pediatr Clin North Am, 51: 389, 2004 Yamada, S., Zinke, D. E. and Sanders, D.: Pathophysiology of tethered cord syndrome. J Neurosurg, 54: 494, 1981 Pang, D. and Wilberger, J. E.: Tethered cord syndrome in adults. J Neurosurg, 57: 32, 1982 Yamada, S., Won D. J. and Yamada, S. M.: Pathophysiology of tethered cord syndrome: correlation with symptomatology. Neurosurg Focus, 16: E6, 2004 Keating, M. A., Rink, R. C., Bauer, S. B. et al: Neuro-urological implications of changing approach in management of occult spinal lesions. J Urol, 40: 1299, 1988 Satar, N., Bauer, S. B., Scott, R. M. et al: Late effect of early surgery on lipoma and lipomeningocele in children less than 1 year old. J Urol, 157: 1434, 1997 Palmer, L. S., Richard, I. K. and William, E.: Subclinical changes in bladder function in children presenting with neurological symptoms of the tethered cord syndrome. J Urol, 159: 231, 1998 Flanigan, R. C., Russell, D. P. and Walsh, J. W.: Urologic aspects of tethered cord. Urology, 33: 80, 1989 Kondo, A., Kato, K., Kanai, S. and Sakakibara, T.: Bladder dysfunction secondary to tethered cord syndrome in adults: is it curable? J Urol, 135: 313, 1986 Rosen, R., Buonomo, C., Andrade, R. and Nurko, S.: Incidence of spinal cord lesions in patients with intractable constipation. J Pediatr, 145: 409, 2004 Nogueira, M., Greenfield, S. P., Wan, J., Santana, A. and Li, V.: Tethered cord in children: a clinical classification with urodynamic correlation. J Urol, 172: 1677, 2004 Sillen, U.: Bladder function in infants. Scand J Urol Nephrol Suppl, 215: 69, 2004 Dator, D. P., Hatchett, L., Dyro, F. M., Shefner, J. M. and Bauer, S. B.: Urodynamic dysfunction in walking myelodysplastic children. J Urol, 148: 362, 1992 Sillen, U., Hansson, E., Hermansson, G., Hjalmas, K., Jacobsson, B. and Jodal, U.: Development of the urodynamic pattern in infants with myelomeningocele. Br J Urol, 78: 596, 1996
Purpose: Tethered cord syndrome encompasses a group of clinical symptoms caused by abnormal spinal cord fixation. We evaluated a select cohort of patients with primary tethered cord syndrome in regard to urodynamic and clinical outcome after cord release. Materials and Methods: We retrospectively reviewed the records of patients with the diagnosis of tethered cord from May 2001 to October 2004. Patients were assessed preoperatively by standard urodynamic studies, which was repeated a mean of 6.4 months after tethered cord release. Clinical and urodynamic outcomes were analyzed. Results: Ten male and 14 female patients 1 month to 12 years old (median age 6 years) were evaluable. Preoperatively 14 of the 24 patients with a median age of 8.1 years were toilet trained and 7 (50%) had diurnal incontinence. Constipation was noted in 10 of 24 patients (42%) and urinary tract infections developed in 6 (25%). Postoperatively only 1 patient (7%) experienced diurnal incontinence (p ⫽ 0.04). Constipation was observed in 6 patients (25%) and urinary tract infections developed in 1 (4.2%) (p ⫽ 0.29 and 0.07, respectively). Ten of the 21 children (48%) with abnormal urodynamics had normalized studies postoperatively. Ten of the 17 patients with neurogenic detrusor overactivity achieved normalization and 7 remained unchanged. Two of 3 patients with normal preoperative urodynamics had neurogenic detrusor overactivity and 1 had poor bladder compliance. Four patients with low bladder capacity and/or low compliance preoperatively did not improve. Conclusions: Our results suggest that tethered cord release is beneficial in terms of clinical and urodynamic outcomes. Patients with abnormal urodynamics had 48% improvement after tethered cord release. Neurogenic detrusor overactivity seems to respond better with 59% improvement in urodynamics. The level of the conus on magnetic resonance imaging did not seem to be predictive of urodynamic outcome. Patients with a normal bladder may show urodynamic deterioration postoperatively, which raises cause for concern. Key Words: spinal cord, urodynamics, neurogenic bladder, spinal dysraphism
ccult spinal dysraphism (primary TC) refers to a select group of spinal abnormalities associated with a posterior bony spinal defect that develops beneath an intact dermis and epidermis.1 It includes spinal and caudaequina lipoma, diastematomyelia, lipomyelomeningocele, dorsal dermal sinus, neural enteric cyst and filum terminale syndrome. Spinal cord tethering may also be secondary to surgery or infection. Developmental anomalies of the spinal cord often result in neurological bladder dysfunction. The most common and widely recognized of these anomalies is myelomeningocele, which is associated with neurogenic vesical dysfunction in more than 90% of patients.2 TC syndrome refers to a group of clinical symptoms caused by abnormal spinal cord fixation. When the spinal cord is tethered, there is a limitation of its motion, which may lead to ischemic damage of the
O
Study received Institutional Review Board approval. * Correspondence and requests for reprints: Department of Urology, Children’s Hospital of Eastern Ontario, 401 Smyth Rd., K1H 8L1, Ottawa, Ontario, Canada (e-mail: [email protected]). † Financial interest and/or other relationship with Q-Med Canada. ‡ Financial interest and/or other relationship with Canadian Medical Association and Medico-Legal Conference.
0022-5347/06/1764-1729/0 THE JOURNAL OF UROLOGY® Copyright © 2006 by AMERICAN UROLOGICAL ASSOCIATION
neural tissue secondary to neural root stretching. It is well documented that children may present with neurological, orthopedic, dermatological and urological manifestations of TC syndrome.3 Although some published series of TC release show contradictory results,4 many groups have documented the benefit of TC release in children with subsequent improvement in clinical and urodynamic parameters.2–5 Fone et al found surgery to be beneficial in a group with primary TC and no improvement when releasing secondary tethered cords.2 We evaluated a select group of patients with primary TC syndrome in regard to urodynamic and clinical outcomes.
MATERIALS AND METHODS We performed an Institutional Review Board approved, retrospective review of the records of patients with a clinical diagnosis of TC due to spinal dysraphism who were referred for urodynamic evaluation from May 2001 to October 2004. All patients underwent TC release, as performed by the neurosurgery team at our institution. The children were assessed preoperatively with UDS, which was repeated a mean of 6.4 months after TC release. Clinical and urodynamic outcomes were compared between the 2 periods. The diagnosis of TC was based on history and
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Vol. 176, 1729-1732, October 2006 Printed in U.S.A. DOI:10.1016/j.juro.2006.03.116
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physical examination, and all children underwent spinal cord MRI. Complete urological evaluation was done, including ultrasound of the upper tract. Intraoperative urodynamics were used to guide the manipulation of nerve roots and avoid injury to the lower urinary tract innervation. Intravesical and intrarectal pressure were recorded using standard urodynamic equipment and pelvic floor muscle activity was monitored during surgery with electromyography and intrarectal electrodes. Clinical outcomes were evaluated for the last 6-month period preoperatively and for a mean followup of 6 months after surgery. Clinical outcomes were urinary and fecal incontinence, constipation, UTI, and the use of oxybutynin, antibiotic prophylaxis and CIC. UDS parameters evaluated were total bladder capacity, pressure at total bladder capacity, compliance, neurogenic detrusor overactivity, post-void residual urine volume and detrusor leak point pressure. Differences in dichotomous outcomes preoperatively vs postoperatively were assessed using the McNemar chisquare test with a continuity correction. The CI for these differences was calculated using the normal approximation with a continuity correction. RESULTS A total of 24 patients were included in this study, including 10 males and 14 females 1 month to 12 years old (median age 6 years). All patients were ambulatory and diagnosed with occult spinal dysraphism. Patients with TC and a history of spinal cord surgery, trauma or TC secondary to infectious conditions were excluded. Table 1 lists lower back findings, lower limb complaints and MRI findings in our patient population. Incontinence and UTI were the most common urinary symptoms, while constipation was the most frequent intestinal complaint. Table 2 shows clinical outcomes after surgery. Preoperatively 14 of 24 patients (58%) were toilet trained and they had a median age of 8.1 years (range 3 to 12), while 10 (42%) who were not toilet trained had a median age of 8 months (range 1 to 12). Seven of the 14 toilet trained patients (50%) had daytime incontinence associated with urgency and frequency preoperatively and only 1 (7%) remained incontinent after surgery. All 7 patients who were
TABLE 1. Patients with abnormal lower back examination, lower limb complaints and MRI findings No. Pts (%) Lower back examination: Skin dimple/gluteal cleft asymmetry Hemangioma ⫹ hair tuft Sacral fat pad Small meningocele (micro meningocele) Scoliosis Normal Lower limb complaints: Gait abnormality Pain Weakness/numbness 1 Leg smaller 1 Foot smaller None MRI findings: Thickened filum Lipoma Syrinx Spina bifida occulta Diastematomyelia (split cord malformation.)
24 9 (37) 5 (21) 3 (13) 2 (8) 2 (8) 3 (13) 4 (17) 3 (13) 2 (8) 2 (8) 2 (8) 11 (46) 9 (37) 9 (37) 8 (33) 5 (21) 4 (17)
TABLE 2. Preoperative and postoperative clinical and urodynamic parameters
No. clinical outcome/total No. (%): Daytime incontinence* Constipation UTI Oxybutinin CIC Urodynamic outcome: Mean bladder capacity ⫾ SD (ml) Mean bladder capacity pressure ⫾ SD (cm H2O) Mean compliance ⫾ SD (ml/cm H2O) No. neurogenic detrusor overactivity Mean ml post-void residual urine vol (% bladder vol)
Preop
Postop
7/14 (50) 10/24 (42) 6/24 (25) 2/24 (8) 2/24 (8)
1/14 (7) 6/24 (25) 1/24 (4) 2/24 (8) 3/24 (12)
103.9 ⫾ 68.2 36.2 ⫾ 28.6
148.6 ⫾ 89.7 17.2 ⫾ 25.4
5.8 ⫾ 5.2 17 19.6 (18.2)
23.6 ⫾ 19.9 11 4.7 (3.1)
* Assessed only in toilet trained patients (older than 3 years).
continent preoperatively remained continent following surgery. Thus, only 1 of the 14 patients (7.1%) was incontinent following surgery (p ⫽ 0.04). The change was – 42.9% (95% CI – 82.8% to –2.9%). In the total group constipation was present in 10 of 24 patients (42%) preoperatively, of whom only 4 continued to experience constipation following surgery. Two of the 14 patients who did not experience constipation preoperatively experienced constipation following surgery. Thus, 6 patients (25.0%) experienced constipation postoperatively (p ⫽ 0.29). The change was ⫺16.7% (95% CI – 46.9% to 13.6%). Preoperatively UTI was present in 6 of the 24 patients (25.0%) and following surgery only 1 of the 6 had UTI. None of the 18 patients who were free of UTI preoperatively had UTI following surgery. Thus, only 1 of the 24 patients (4.2%) had UTI following surgery (p ⫽ 0.07). The change was –20.8% (95% CI ⫺45.2% to 3.6%). None of the 24 patients had stool soiling. Two children were on oxybutynin and CIC. No patient was on antibiotic prophylaxis. The 2 patients on oxybutynin orally continued the drug postoperatively. Two patients on CIC preoperatively continued in the postoperative period and another was started on CIC due to a low compliant bladder. Table 2 lists preoperative and postoperative urodynamic parameter changes. UDS was performed an average of 6.4 months after TC release. There was no patient with an areflexic detrusor before or after surgery in our series. To facilitate analysis we grouped urodynamic patterns as hyperreflexic, low compliance/capacity and normal bladders. Of the 24 patients 17 had a hyperreflexic bladder, including 10 (59%) in whom the pattern normalized, 6 who remained unchanged and 1 in whom a low compliance bladder developed. Four of the 24 patients had low bladder capacity and/or compliance, and no improvement after TC release. Three of the 24 patients had normal preoperative UDS, of whom 2 had a hyperreflexic bladder and 1 had poor bladder compliance. Thus, overall 21 of the 24 patients (87.5%) had some UDS abnormality preoperatively compared to 14 (58.3%) postoperatively (p ⫽ 0.10). The change was ⫺29.2% (95% CI ⫺64.4% to 6.0%). Considering the outcome in these 21 patients who had UDS abnormality preoperatively 10 (48%) improved after TC release, of whom all had neurogenic detrusor overactivity. Of the 24 patients 17 (71%) had the conus medullaris at L3 or below, while 7 (29%) had the conus at L1 or L2. Of the
TETHERED CORD RELEASE FOR OCCULT SPINAL DYSRAPHISM 17 patients with neurogenic detrusor overactivity preoperatively 14 (82%) had the conus medullaris at or below L3 before surgery, while only 3 (18%) had the conus at L1-L2. Postoperatively 7 of the 10 patients (70%) with neurogenic detrusor overactivity in whom UDS normalized had the conus at L3 or below. Three patients had split cord malformation (diastematomyelia) and only 1 had a normalized UDS. Two patients presented with progressive and worsening scoliosis, and neither responded to TC release. When we stratified patients by age, there was no statistically significant difference in these clinical and urodynamic outcomes. DISCUSSION The lesions of neural tube defects are variations of the normal development of the spine and spinal cord. Knowledge of the normal embryology allows better understanding of these defects and the anatomical relationships seen on diagnostic studies.6 A number of pathological conditions have been described under the label of spinal dysraphism, including congenital anomalies of the caudal spinal cord and distal vertebral column. They do not result in an open vertebral canal. Because they are defects covered by skin and subcutaneous tissue, many groups refer to them as occult dysraphism. Classically the lower part of the conus medullaris should lie at L1-L2 and the normal filum terminale should be less than 2 mm wide at the L5-S1 level. There has been some discussion as to whether a normal level conus medullaris could be tethered without lying in a low position on MRI. Our series showed that 17 of 24 patients (71%) had a conus at L3 or below. Only 7 of these 17 patients (41%) with a low conus preoperatively had normal UDS postoperatively. Seven children had the conus at the normal L1-L2 level and 3 (42%) had a good response. Thus, the position of the conus alone was not a factor predictive of outcome in the entire patient cohort and some patients with a normal conus on MRI benefited from TC release. In TC syndrome the distal lumbar spinal cord is fixed at 2 points, that is 1 at the site of tethering and the other at the level of the exit of the nerve roots. During extension, flexion or the abdominal Valsalva maneuver there is a lack of motion and stretching of the cord and roots, which can lead to ischemia and an anaerobic metabolism.7 The clinical findings of TC result from the cumulative damage of intermittent neuronal hypoxemia.8,9 Because interneuronal axon connections require an aerobic metabolism, they are the first affected and clinically this leads to urinary incontinence and a decreased skeletal muscle reflex. In contrast, the long neuronal tracts involving muscular movement are less susceptible to hypoxic injury and, hence, the findings of lower limb weakness with associated hyperreflexia and an upward Babinski reflex are delayed manifestations of neurological impairment.8 UDS is can anticipate neurological bladder dysfunction secondary to TC and it is often done. Loss of the sacral reflex arc and the development of neurogenic detrusor overactivity are the earliest alterations that can be detected by physical and urodynamic examinations. In this study patients with neurogenic detrusor overactivity on preoperative UDS were the only ones who responded favorably to TC release. Of these 17 patients 14 (82%) had the conus at a low position at L3 or below. When we correlated neurogenic detrusor overactivity and the level of the conus with normal UDS postoperatively, there was a 50% response (7 of 14
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patients) for the conus at or below L3 and a 100% response (3 of 3) for the conus at L1 and L2. These findings may show that, although a lower conus is unquestionably pathological, patients with neurogenic detrusor overactivity and a normal level conus may also have a significant pathological condition and they may respond to TC release. This may suggest that such patients with a normal level conus have a less severe form of cord tethering with decreased end organ damage. The presence of syrinx, lipoma, diastematomyelia or thick filum on MRI were not predictive of postoperative outcome in this study. Newborns and infants evaluated for possible TC usually have a normal neurological examination. Urodynamic studies show an abnormality in approximately a third of infants and children younger than 18 months.10,11 Urinary symptoms do not seem to be consistently present but when they manifest they are usually secondary to neurogenic detrusor overactivity, leading to incontinence, urgency and urinary frequency. Less frequently one can detect detrusor sphincter dyssynergia on UDS. Palmer et al found occult changes in the bladder in 75% of children with myelodysplasia who did not have clinical manifestations of TC syndrome referable to the urinary tract.12 The indication for surgical treatment for TC is often a challenging decision. MRI and US are not completely reliable for assessing the filum terminale and currently to our knowledge there is no test to confirm metabolic suffering of the neuronal cell. It is still unclear if all children with neurological signs of TC experience deterioration if the cord is not untethered. The literature contains several small series of the pros and cons of surgery. To our knowledge there are no proven long-term data to predict which patient may benefit from the procedure or whether the unreleased cord would neurologically deteriorate with time. More worrisome is the fact that 10% of patients with a normal bladder have neurogenic bladder after surgical untethering.10 Unfortunately there is no strong evidence to answer these uncertainties. Most neurosurgeons rely on their clinical judgement and experience to decide whether to intervene. Daytime urinary incontinence is a bothersome symptom that impairs quality of life. In our series it was present in 50% of the children and it dramatically improved, decreasing to 7% after cord untethering. Neurogenic detrusor overactivity bladder had the highest response rate among urodynamic parameters with resolution in 59% of cases. Similar results were reported by Khoury et al in a group of 31 select children with TC who had occult dysraphism.5 They noted 72% improvement in urinary incontinence after releasing the cord and 59% resolution of neurogenic detrusor overactivity.5 Unlike the data reported by Flanigan13 and Kondo14 et al showing that 71% and 60% of patients with TC, respectively, had an acontractile detrusor, we had no patient with this bladder pattern in our study. There is great controversy about the most common pattern of UDS in TC and the result reported by Kondo et al was among in adult population. Detrusor-sphincter dyssynergia is not commonly described in these patients. Constipation is not frequently referred in the literature as associated with tethered cord. Rosen et al noted that only 9% of children with spinal cord abnormalities had intractable constipation but TC was the most common association.15 We found constipation in 42% of our patients, which decreased to 25% after surgery. A decrease in UTI from 25% to
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TETHERED CORD RELEASE FOR OCCULT SPINAL DYSRAPHISM
4% may have been related to a decrease in post-void residual urine from 18% to 3% of total bladder volume, which was associated with improvement in intestinal constipation or bladder function after TC release. Mean bladder capacity improved from 103.9 to 148.6 ml after surgery, representing a 43% increase in bladder storage volume. Similar improvement was observed in mean bladder compliance, which increased from 5.8 to 23.6 ml/cm H2O. Improved bladder compliance is the result of better vesical function after surgery and it may reflect reversibility of the neural lesion. Keating10 and Kondo14 et al reported better results when TC is identified and released early and they emphasized the necessity of correction before the lesion becomes permanent. In our series age at surgery was not predictive of a better outcome. Surgery to untether the spinal cord is not without risk. In fact, a 12% risk of deterioration was observed postoperatively in patients with normal preoperative UDS in 1 reported series.10 We observed a higher rate of bladder deterioration. Two of the 3 patients with a normal bladder on UDS preoperatively had neurogenic detrusor overactivity and 1 had a low compliance pattern on postoperative evaluation. In our series bladders with low capacity and low compliance did not benefit from surgery. We postulate that this may reflect a structural end stage organ lesion with collagen deposition in place of normal smooth muscle. If further studies confirm this finding, we should consider avoiding TC release in such children. Two patients with neurogenic detrusor overactivity, who were on CIC, and oral and intravesical oxybutynin preoperatively, continued with the same treatment after surgery. One child had an excellent response with bladder capacity increasing from 77 to 189 ml, although compliance increased less, that is from 12 to 17 ml/cm H2O. In the other child treatment failed with preoperative and postoperative compliance of 3 and 4.1 ml/cm H2O, respectively. A male patient with neurogenic detrusor overactivity and a compliance of 1.2 ml/cm H2O preoperatively began CIC after surgery but followup UDS showed a normal pattern with a compliance of 20 ml/cm H2O. Our study has limitations related to its retrospective analysis and inherent bias. There have been several reports of UDS parameters associated with neurological disease in the pediatric population.16 –19 However, the definition of normal UDS in a child who is not toilet trained is a challenging situation that may create definition bias in the results. Although our sample was small and we had limited power to detect changes, our results suggest that TC release is beneficial in terms of clinical and urodynamic outcomes. CONCLUSIONS Our results suggest that TC release is beneficial in terms of clinical and urodynamic outcomes. Patients with abnormal urodynamics had 48% improvement postoperatively. Children with neurogenic detrusor overactivity seem to respond better with 59% improvement in UDS. The level of the conus on MRI and age at intervention did not seem to be predictive of the urodynamic outcome. Low capacity/poorly compliant bladders did not benefit urodynamically from this intervention. Patients with a normal bladder may show urodynamic deterioration postoperatively, which raises cause for concern.
Abbreviations and Acronyms BC BV CIC MRI TC UDS US UTI
⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽ ⫽
bladder capacity bladder volume clean intermittent catheterization magnetic resonance imaging tethered cord urodynamic study ultrasound urinary tract infection
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