Journal of Pediatric Urology (2014) 10, 627e633

Predictors of urinary continence following tethered cord release in children with occult spinal dysraphism Brendan T. Frainey*, Elizabeth B. Yerkes, Vani S. Menon, Edward M. Gong, Theresa A. Meyer, Robin M. Bowman, David G. McLone, Earl Y. Cheng Division of Urology, Ann & Robert H. Lurie Children’s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, USA Received 8 March 2014; accepted 23 June 2014

Available online 10 July 2014

KEYWORDS Spinal dysraphism; Occult; Tethered cord syndrome; Filum terminale; Urodynamics; Urinary incontinence

Abstract Objective: Children with occult spinal dysraphism represent a wide spectrum of patients. Previous studies assessing urologic outcomes have in part been deficient due to the inability to appropriately categorize these patients and gather long-term follow-up data. In this study, a uniform set of patients that had occult spinal dysraphism with magnetic resonance imaging findings of a fatty filum terminale (FF) and/or low-lying cord (LLC) was identified. Utilizing long-term follow-up data, predictors for achieving urinary continence following tethered cord release (TCR) were determined. Methods: A retrospective chart review of pediatric patients with a diagnosis of tethered cord who underwent TCR from 1995 to 2005 was performed. Analysis was limited to patients who had primary TCR by one of two neurosurgeons within our multidisciplinary spina bifida clinic, who had greater than 1-year follow-up, and who were old enough to have continence status assessed (age > 6 years unless definitively toilet trained earlier). Patients with other associated forms of spinal dysraphism (lipomyelomeningeocele, spinal lipomas, sacral agenesis), anorectal malformations, and genitourinary anomalies were excluded. Pre- and post-TCR urodynamics, radiographic studies, functional orthopedic status, and urologic outcomes were assessed. Urodynamic results were categorized by three blinded urologists into one of three urodynamic patterns: (1) normal, (2) indeterminate, and (3) high risk. Results: A total of 147 patients with FF and/or LLC that underwent TCR were reviewed. 51 patients were excluded because of another associated spinal dysraphism (15/51 patients) or an anorectal/genitourinary anomaly (36/51 patients). Fifty-nine of the remaining 96 patients had adequate long-term follow-up data to be included in the study. 20 patients were asymptomatic at the time of TCR while 39 presented with orthopedic and/or urologic symptoms. The average

* Corresponding author. Ann & Robert H. Lurie Children’s Hospital of Chicago, 225 E. Chicago Ave., Box 24, Chicago, IL 60611, USA. Tel.: þ1 630 400 0410; fax: þ1 312 227 9457. E-mail addresses: [email protected], [email protected] (B.T. Frainey). http://dx.doi.org/10.1016/j.jpurol.2014.06.008 1477-5131/ª 2014 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.

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B.T. Frainey et al. age at surgery was 59.3 months (range 2e277 months) with an average follow-up of 7.0 years (range 1e16 years). At latest follow-up, 47 (80%) patients were continent while 12 (20%) were either incontinent or utilizing clean intermittent catheterization (CIC). Statistical analysis revealed that age of untethering, type of cutaneous lesion, level of conus, presence of hydronephrosis, and high-grade vesicoureteral reflux (VUR) were not independent predictors of continence. In patients with a cutaneous lesion who were asymptomatic, 19/20 obtained continence post-TCR (*p Z 0.036). In patients who were old enough to assess continence pre-TCR, 14/25 patients were continent pre-TCR and 11/25 were incontinent. Of the 14 who were continent pre-TCR, all remained continent post-TCR (*p Z 0.002). Of the 11 who were incontinent pre-TCR, five (45%) eventually became continent post-TCR. Assessment of urodynamic data revealed that neither pre- nor post-TCR urodynamics predicted continence status. Conclusion: Isolated cutaneous lesions and preoperative continence status are positive predictors for post-TCR continence. While pre- and post-TCR urodynamics do not predict continence status, their utility in preoperative work-up, monitoring for retethering, and long-term urologic follow-up requires further examination. ª 2014 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.

Introduction Controversy exists regarding the indications to operate on patients with a tethered spinal cord as well as the appropriate timing for surgical tethered cord release (TCR) [1e3]. In patients who do become symptomatic, the constellation of clinical symptoms that develop are referred to as tethered cord syndrome (TCS). The development of symptoms can occur at any age causing a wide array of symptoms that can be neurological, orthopedic, and/or urologic in nature. In children, new-onset urinary incontinence or an inability to toilet train may be one of the first indicators of TCS. In such patients with TCS, prompt surgical TCR is widely accepted to prevent worsening of symptoms and to potentially reverse those that are already present [1,3]. Occult spinal dysraphism (OSD) encompasses several abnormalities that occur due to incorrect or incomplete development of the neural tube and are associated with a tethered cord. Children born with OSD are not only believed to be anatomically tethered based on radiographic findings, but also have an inherent risk of developing symptomatic TCS. Included within the spectrum of OSD are abnormalities such as fatty filum terminale, spinal lipoma, lipomyelomeningocele, diastematomyelia (split cord malformation), neurenteric cyst, and terminal syringohydromyelia [4]. To date, there are no studies that adequately examine factors that influence the attainment of urinary continence in children with TCS following TCR. Furthermore, studies on TCS and OSD often lump the various forms of OSD into a single grouping [5e9]. Failure to distinguish between the different forms of OSD may lead to inaccurate assumptions regarding prognosis and treatment for specific groups of patients. Thus, there exists a need to better determine urologic outcomes within the specific subtypes of OSD. In this study, a uniform subset of OSD patients with magnetic resonance imaging (MRI) findings of a fatty filum terminale (FF) and/or low-lying cord (LLC) was identified. These two subtypes of OSD are commonly seen in association with one

another and typically represent a more uniform population within OSD. This study did not seek to determine the need for TCR or the appropriate timing for surgical TCR in this subset of patients. Rather, utilizing long-term follow-up data, this study simply sought to identify predictors for achieving urinary continence in patients with FF and/or LLC following TCR.

Methods Data of pediatric patients with a diagnosis of FF and/or LLC who underwent primary TCR from 1995 to 2005 at our institution were retrospectively reviewed. Analysis was limited to patients who were old enough for continence status to be assessed at latest follow-up (age  6 years unless definitively toilet trained earlier). At least 1 year of follow-up post-TCR was also required for inclusion in the study. Patients with other associated forms of OSD (lipomyelomeningocele, spinal lipoma, anterior meningocele, diastematomyelia, and dermal sinus tract) or anorectal malformations/genitourinary anomalies (VACTERL association, imperforate anus, cloacal anomalies, sacral agenesis) were excluded. Baseline characteristics including sex, age at TCR, MRI findings, presenting symptoms, presence of a global, confounding diagnosis, and level of the conus were recorded. Pre- and post-TCR evaluation of urodynamics, radiographic studies, and urologic, orthopedic, and gastrointestinal function were also assessed. The primary outcome examined was the ability or inability to achieve urinary continence following TCR. All preoperative MRIs were interpreted by both a radiologist and neurosurgeon. The exact level of the conus was identified and considered normal when it was located superior to the midpoint of the L2 vertebrae and was considered low-lying when below this point. All patients then underwent subsequent tethered cord release. After a laminotomy, the filum was exposed intradurally under microscopic guidance, cauterized, and transected, thereby

Predictors of urinary continence following tethered cord release in children with OSD untethering the cord. Pre- and post-orthopedic status was also recorded. Pre- and post-TCR urinary and bowel status were determined based on urologist assessment of the patient’s clinical history. In this urinary assessment, continence status, need for clean intermittent catheterization (CIC), and urinary tract infection history were recorded. Incontinence was defined as continued wetting/leaking urine or utilization of CIC, regardless of whether leakage occurred between catheterizations. Renal ultrasound and voiding cystourethrogram data were also acquired when available. In the evaluation of urodynamic studies, we utilized a unique urodynamic classification scheme that is regularly used in our clinic. This classification scheme is based on definitions set forth by the International Children’s Continence Society and has three main categories: (1) normal, (2) indeterminate, and (3) high risk. Estimated bladder capacity (EBC) was calculated by the formula [(1 þ age in years)  30] milliliters for those aged 2e11 years old and by the formula [weight (kg)  7] milliliters for children less than 2 years of age. Within each category, patients were further subcharacterized by residual urine. Abnormal was defined as >20 mL by post-void residual as per International Children’s Continence Society definitions. Normal was defined as having a compliant filling curve, normal bladder capacity, and efficient voiding contraction with adequate emptying of the bladder. High risk was defined as having a pressure-specific bladder capacity that is 30 cm water at or before 50% expected capacity for age, clear evidence of detrusor sphincter dysynnergia (DSD), or leak point pressure 40 cm water. Within the indeterminate category (2), four sub-classifications were created: 2a: normal filling curve with high voiding pressures (greater than 100 cm of water); 2b: prominent detrusor overactivity (2 contractions > 15 cm water); 2c: underactive bladder (inefficient voiding contraction); and 2d: sustained inefficient contraction or progressive rise in pressure with late leak (Table 1). Statistical analyses were performed using the Student t test and Pearson chi-Square test on the SPSS software package (Version 12.0). A p-value 15 cm water

2c Detrusor underutilization: normal filling curve with inefficient voiding contraction (30 cm water at or before 50% expected capacity for age), definitive detrusor sphincter dyssynergia (DSD), or leak point pressure 40 cm water

Presenting symptoms Thirty-nine out of 59 patients (66%) presented with orthopedic and/or urologic symptoms. Urologic symptoms included enuresis, recurrent urinary tract infection, voiding complaints, and high-grade vesicoureteral reflux. Orthopedic symptoms included lower extremity pain, back/ buttock pain, gait abnormality, or progression of an

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B.T. Frainey et al.

Figure 1

Inclusion criteria.

orthopedic diagnosis (scoliosis, clubfoot, or vertical talus). The average age at TCR of the symptomatic group was 80.7 months (range 4.2e276.6 months). Of the 39 symptomatic patients, five (8%) presented with urologic symptoms, 10 (17%) with orthopedic symptoms, and 24 (41%) with some combination of orthopedic and urologic symptoms. In the symptomatic group, no correlation was found between specific symptoms and post-TCR urinary status. Conversely, 20 out of 59 patients (34%) were completely asymptomatic prior to TCR, with the presence of a cutaneous lesion(s) as the only indicator of a tethered cord. Cutaneous lesions included an atypical sacral dimple, hemangioma, hairy patch, or an asymmetrical gluteal fold. The average age of the asymptomatic group at the time of surgery was 17.8 (range 2.3e72.7 months). In the asymptomatic group, 19 out of 20 (95%) attained urinary continence following TCR. This was found to be statistically significant (*p Z 0.036). The one patient who did not achieve continence in this group was a female with a sacral dimple who was born with a chromosomal abnormality and developmental delay. Subgroup analysis was completed on asymptomatic patients with a cutaneous lesion, but without associated global diagnoses that could affect continence attainment (cerebral palsy, developmental delay, chromosomal abnormalities, etc.). Five out of 20 patients were found to have an associated global diagnosis. Of the remaining 15 patients without a global diagnosis, all 15 went on to achieve continence post-TCR. Analysis of the specific type of

cutaneous lesion did not reveal any significant correlation with post-TCR continence status.

MRI findings MRI findings were utilized to establish a radiographic diagnosis and the position of the conus prior to TCR. The most common radiographic diagnosis was fatty filum terminale (FF) in combination with a low-lying cord (LLC) in 29 (49%), followed by FF alone in 26 (44%), and LLC alone in 4 (7%). At latest follow-up, 24 out of 29 patients with FF þ LLC achieved continence, 20 out of 26 patients with FF alone achieved continence, and three out of four patients with LLC alone achieved continence. No significant correlation was found between the type of radiographic diagnosis and post-TCR continence status (p Z 0.841). A similar analysis was conducted regarding conus position. At latest follow-up, 21 out of 26 (81%) patients with a normally positioned conus (superior to the midpoint of L2) and 26 out of 33 (79%) patients with a low-lying conus (inferior to the midpoint of L2) attained continence postTCR (p Z 0.851). Additional subgroup analyses were also completed to potentially correlate specific conus positions with post-TCR continence as opposed to defining the conus as “normally positioned” versus “low-lying.” No significant correlation was found between specific conus positions and post-TCR continence.

Predictors of urinary continence following tethered cord release in children with OSD Table 2

Urodynamics

Predictors of urinary continence. Post-op continence status

p

Continent Incontinent Total Sex M F MRI findings FF only LLC only FF þ LLC Age at TCR (months) Presenting symptoms Asymptomatic (cutaneous lesion only) Symptomatic (urologic, ortho, neuro) Pre-op continence status Continent Incontinent Pre-op urodynamics Normal Indeterminate High risk Post-op urodynamics Normal Indeterminate High risk Pre-op VCUG Normal/low-grade VUR (1e3) High-grade VUR (4e5) Pre-op US Normal/low-grade HN (1e3) High-grade HN (4)

47 (80%)

12 (20%)

22 25

4 8

20 3 24 58.0

6 1 5 64.4

19

1

28

11

14 5

0 6

19 22 1

4 5 1

631

0.401

0.841

0.750 0.036*

0.002*

A total of 207 urodynamic studies were evaluated and categorized by the consensus of three blinded urologists. 52 patients (88%) had urodynamics pre-TCR. Of the preoperative studies, 23 were regarded as normal while two were high risk. The remaining 27 studies fell into the indeterminate categorization within the four previously described subcategories (2a, 2b, 2c, 2d). Forty-nine patients (83%) had post-TCR urodynamics for evaluation. Of the post-operative studies, 18 were deemed normal and three high risks. Similar to the preoperative urodynamic breakdown, the majority of the studies (28) were indeterminate (Table 3). Statistical analysis revealed that neither pre- nor postTCR urodynamics were correlated with post-TCR urinary continence. However, post-operative urodynamics approached significance with p Z 0.087. Multiple subgroup analyses were also completed, analyzing each specific preand post-operative urodynamic pattern. No significant correlations were noted between specific urodynamic patterns and long-term urinary continence following TCR.

0.547

Urological radiographic imaging

0.087 16 20 1

2 8 2

9 1

3 2

21 0

6 1

0.171

0.078

VUR Z vesicoureteral reflux; VCUG Z voiding cystourethrogram; FF Z fatty filum terminale; LLC Z low-lying cord. * e indicates a statistically significant p-value.

Preoperative continence status Preoperatively, 25 patients were either continent or old enough to expect continence. Fourteen out of 25 patients were continent, while 11 of 25 were incontinent. Of those 11, nine were persistently wetting/leaking urine despite time voiding and two were utilizing CIC. The average age of these 25 patients was 9.8 years (range 5e23.1 years). The remaining 34 patients were not old enough for continence status to be assessed prior to TCR. The average age of this group was 1.4 years (range 0.2e5.5 years). All 14 patients that were continent preoperatively remained continent long-term following TCR (*p Z 0.002). Of the 11 incontinent pre-TCR, five (46%) were eventually able to achieve continence post-TCR, while 6 (54%) remained incontinent following surgery. In the 34 patients for which continence status could not be assessed preoperatively, 28 (82%) went on to become continent post-TCR, whereas six (18%) never achieved continence as of latest follow-up (3 on CIC).

Pre-TCR renal ultrasonography (RUS) and pre-TCR voiding cystourethrogram (VCUG) were also assessed in patients with available imaging. Pre-TCR, RUS was performed in 28 patients (47%) and VCUG results were available for 15 patients (25%). The relationship between RUS grade and postTCR continence yielded a p-value that approached significance (p Z 0.078), whereas the relationship between preTCR vesicoureteral reflux severity and post-TCR continence was not found to be statistically significant (p Z 0.171).

Discussion For patients with OSD undergoing TCR, it can often be difficult to predict the urological outcome of patients regarding continence. No research to date has adequately studied predictors for attaining urinary continence following TCR. Furthermore, a deficiency in long-term data regarding specific diagnoses within the OSD spectrum is recognized. Therefore, this study sought to identify predictors for urinary continence in a specific subset of patients with OSD undergoing TCR, namely those with an MRI diagnosis of FF/LLC. This was done so that accurate

Table 3

Urodynamic results.

Classification

Pre-op

Post-op

Latest

Normal (1) Indeterminate (2) 2a 2b 2c 2d High risk (3) Not available

23 28 2 8 6 12 2 6

18 28 4 9 6 9 3 10

24 23 2 6 6 9 2 10

632 assumptions about prognosis and further treatment within this population can be made. From this study, several positive predictors for continence were identified. First, the presence of a cutaneous lesion in an otherwise asymptomatic child was found to be highly predictive of achieving continence following TCR for FF/LLC. Specifically, 95% of the patients who were asymptomatic preoperatively were also continent post-TCR (*p Z 0.002), as opposed to those patients who presented with some form of symptomatology in which only 67% were continent post-TCR. To date, no studies have identified the presence of an isolated cutaneous lesion as a positive predictor for continence following TCR. However, Nogueira et al. [10] did note in their series of patients with tethered cord that 100% of patients who presented with cutaneous lesions and hyperreflexic bladders preoperatively showed resolution of these changes post-TCR. These findings, in conjunction with those from the present study, suggest that asymptomatic patients with cutaneous stigmata have a high likelihood of achieving full continence and resolution of any preoperative bladder instability following TCR. Another factor to consider when evaluating symptomatic versus asymptomatic patients is age at the time of TCR. The average age of the asymptomatic group at the time of surgery was 17.8 months while the average age of the symptomatic group was 80.7 months. Although the difference in age at TCR was not found to be statistically different between the two groups, this lack of statistical significance may be related to the relatively small sample size. The difference in age deserves further evaluation in a larger patient population because the improved rate of continence in the asymptomatic group in combination with the younger age of TCR both support the notion that better clinical outcomes are achieved in children when tethered cord is identified and released early [11,12]. The second significant positive predictor of continence following TCR in these patients was preoperative continence status. All 14 patients who were continent prior to TCR maintained continence long-term following TCR. The average length of follow-up for this group after TCR was 6.9 years. Guerra et al. [6] reported similar findings, in which all seven patients in their series who were continent preoperatively remained continent following TCR. These findings are extremely valuable when counseling patients and families regarding the pros and cons of observation versus surgery for tethered cord since it appears the risk of developing worsening bladder function or incontinence following TCR is minimal. For children who were incontinent in our study prior to untethering, 45% went on to achieve continence at latest follow-up. These findings are not quite as promising as those reported by Khoury et al. [7] and Guerra et al. [6], who report 72% and 86% resolution of daytime incontinence, respectively. However, this disparity in continence rates post-TCR may in part be related to the more diverse patient populations and shorter follow-up in these studies. Regardless, the collective results of these three studies strongly suggest that a large proportion of patients who are incontinent preoperatively will have improvement in their level of continence following TCR. Regarding urodynamics, we utilized a unique classification system for the evaluation of urodynamic studies. This approach differs from many previous studies, which have

B.T. Frainey et al. sought to assess more objective parameters such as bladder capacity, bladder compliance, leak point pressure, detrusor activity, and sphincter dysynnergia [1,9,13e15]. While these objective measurements are important and less subject to individual interpretation biases, it is our experience that assessment of the bladder with these parameters alone may not paint an adequate picture of a patient’s overall bladder dynamics. Furthermore, they often do not depict the true clinical state of the bladder. The novel classification system utilized in this study is based on the “shape of the curve” during filling and emptying, as well as consideration of voiding pressures. When used in conjunction with standard urodynamics measurements, this system has been shown to have great clinical utility in longitudinal follow-up. It is now used regularly in our multidisciplinary spina bifida clinic and is currently being assessed for utility in comparative multi-institutional trials in the assessment of children with a neurogenic bladder. In the present study, we did not find any specific correlation of pre- or post-urodynamics with post-TCR continence. However, post-operative urodynamics did approach statistical significance (p Z 0.087), suggesting a potential for predictive value regarding long-term continence attainment. In their study analyzing urological outcomes following TCR, Macejko et al. [9] also found that pre- and post-operative urodynamics did not correlate with clinical outcomes in children with TCS following TCR [10]. While Macejko’s study may correlate with the findings of the present study regarding the relationship between urodynamics and urologic outcomes, the patient cohort encompassed in their study represented a much more diverse set of patients with OSD, as compared to the specific subset of patients with FF/LLC in this study. In addition, Macejko’s study assessed individual objective urodynamic parameters without taking into consideration the shape of the curve, as was done in the present study. Regardless, it appears that the use of specific urodynamic patterns to predict continence following TCR may not be appropriate. It is important to note that continence in this subset of patients did not require normal urodynamic findings. Thus, it is not correct to assume normal bladder function in a continent patient, since many patients can achieve adequate continence despite the presence of abnormal bladder dynamics. Therefore, additional long-term followup is needed to better understand the pertinence of abnormal urodynamics in a continent patient post-TCR. Despite the lack of correlation between urodynamics and continence status after TCR in patients with a FF/LLC, these results should not be interpreted as a recommendation that urodynamics should not be used in the evaluation and treatment in this unique subset of patients. Although they may not be predictive of continence, pre- and postoperative urodynamics may prove to be vital for the initial assessment of neuropathic bladder dysfunction, follow-up for the development of tethered cord, and guidance of therapy for persistent neurogenic dysfunction. To this end, urodynamics are still routinely used in all patients with OSD. Additional studies are ongoing to better understand their role in the management of patients with other specific forms of OSD and myelomeningocele. Although study design, data collection, and data analysis were carefully conducted, certain limitations within the

Predictors of urinary continence following tethered cord release in children with OSD study remained. Such limitations include the inherent biases associated with a retrospective study. Since this study specifically addressed those patients who had surgery for FF/LL, it does not allow for comparative assessment of continence in patients who have not had surgery. Additionally, some limitations were also present within the urodynamic assessment. For example, the majority of our patients had urodynamics done pre-and post-TCR, but not every patient had both studies performed. Thus, the sample size of patients that could be assessed for post-op urodynamic changes decreased. Finally, interpretation of urodynamics in pediatric patients presents unique challenges, specifically in the determination of artifact versus true bladder function. Further studies to expand upon this research are currently underway. Similar methods and analysis will be applied to patients with other forms of OSD aside from FF/ LL, specifically those with lipomyelomeningocele and spinal lipoma. Additionally, the urodynamic classification system created for this study will be analyzed in greater detail in order to determine whether certain patterns or categorizations can be correlated with post-operative urological outcomes other than continence. Long-term controlled studies that incorporate a non-operative comparison group in the assessment of urologic outcomes in asymptomatic patients with FF/LLC are needed.

Conclusion Isolated cutaneous lesions and preoperative continence status are positive predictors for post-TCR continence in patients with FF/LLC. The identification of these predictors will enhance consultation with patients and families when discussing continence status following TCR. While pre-and post-TCR urodynamics do not significantly predict continence status, their utility in preoperative work-up, monitoring for retethering, and need for further urologic followup requires further examination.

Conflict of interest None.

Funding None.

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Predictors of urinary continence following tethered cord release in children with occult spinal dysraphism.

Children with occult spinal dysraphism represent a wide spectrum of patients. Previous studies assessing urologic outcomes have in part been deficient...
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