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ORIGINAL ARTICLE
Year : 2023 | Volume
: 34
| Issue : 1 | Page : 46-52
The videourodynamic characteristics of patients with chronic spinal cord injury with different injury levels and bladder conditions
Tien-Lin Chang, Hann-Chorng Kuo
Department of Urology, Hualien Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation and Tzu Chi University, Hualien City, Taiwan
Correspondence Address:
Hann-Chorng Kuo
Department of Urology, Buddhist Tzu Chi General Hospital, 707, Section 3, Chung Yang Road, Hualien City
Taiwan
Source of Support: None, Conflict of Interest: None
DOI: 10.4103/UROS.UROS_76_22
Purpose: This study aimed to analyze the association between bladder conditions and Neurogenic lower urinary tract dysfunction (NLUTD) characteristics in patients with spinal cord injury (SCI) with different injury levels using a videourodynamic study (VUDS). Materials and Methods: A single-center, retrospective review of the VUDS database on patients with NLUTD and chronic SCI from 1997 to 2020. A total of 507 patients were enrolled. All patients had a comprehensive chart review, including the injury level, period from diagnosis to VUDS, and VUDS characteristics. Results: The mean age and duration from SCI diagnosis to VUDS were 44.2 ± 15.7 years and 81.8 ± 89.0 months. Detrusor overactivity (DO) was observed in 67.7% of patients and detrusor underactivity (DU) in 26.0%. Bladder outlet obstruction was noted in 78.3% of patients, including detrusor sphincter dyssynergia (DSD) in 53.3% and bladder neck dysfunction in 25.0%. DO and DSD were more commonly observed in patients with suprasacral lesions (P = 0.000 and P = 0.000, respectively), whereas DU had a higher prevalence in patients with lumbar or sacral lesions (P = 0.000). No statistically significant difference was observed in the prevalence of vesicoureteral reflux among different SCI levels. Bladder sensation parameters were more preserved in patients with cervical SCI than in those with lumbar SCI; however, no significant difference in bladder compliance was observed among patients with different SCI levels. Conclusion: The VUDS in patients with SCI revealed a high prevalence of DO, DU, and DSD, which varied among different injury levels. A precise VUDS is necessary for deciding bladder management for patients with SCI and voiding dysfunction.
Keywords: Neurogenic lower urinary tract dysfunction, spinal cord injury, voiding dysfunction
The global incidence of spinal cord injury (SCI) ranges from 8.0 to 246.0 cases per million inhabitants annually. SCI is a common cause of lower urinary tract dysfunction in approximately 70%–84% of patients.[1] It affects the quality of life and results in complications, such as urinary tract infection (UTI), renal stones, bladder stones, vesicoureteral reflux (VUR), hydronephrosis, and renal failure.[2],[3],[4] Bladder management after the initial injury plays an important role in preventing long-term morbidity and mortality. Urinary tract mortality accounts for approximately 13% of patients with SCI due to significant improvement in understanding and management of these diseases.[5] Bladder management includes clean intermittent catheterization, antimuscarinic treatment, and regular urodynamic examination.[6],[7],[8] Hence, early detection of high-risk patients is important.
Neurogenic lower urinary tract dysfunction (NLUTD) commonly develops in patients with SCI. NLUTD causes bladder storage failure due to detrusor overactivity (DO) or urethral incompetence; emptying failure due to detrusor underactivity (DU), bladder neck dysfunction (BND), or detrusor sphincter dyssynergia (DSD); and combined storage and emptying failures due to DSD or DO and impaired contractility.[9] It is difficult to predict bladder and sphincter dysfunctions merely by history and physical examination. Urodynamic evaluation is crucial and necessary for identifying the lower urinary tract status in patients with SCI. Therefore, this study aimed to investigate the association between bladder conditions and NLUTD in patients with chronic SCI and different injury levels.
Materials and MethodsThis is a single-center, retrospective study of patients with chronic SCI and NLUTD between September 1997 and August 2020. Patients were referred to the Urology Department of the hospital for evaluation and management of their voiding or storage urinary tract symptoms. Patients with neurological lesions other than spinal cord diseases and chronic diabetic neuropathy were excluded from the study. Furthermore, patients with combined SCI and central nervous system disorders, such as cerebrovascular accident, parkinsonism, and dementia, were excluded to avoid confusion in the urodynamic interpretation. Patients with acute UTIs, including acute pyelonephritis or acute cystitis, did not proceed to videourodynamic study (VUDS) examination until the UTI was controlled.
The VUDS parameters, including the first sensation of bladder filling (FSF), full sensation (FS), urge sensation (US), bladder compliance, maximum flow rate (Qmax), voiding detrusor pressure at Qmax (Pdet.Qmax), corrected Qmax (cQmax, defined by Qmax divided by the square root of the bladder volume), voided volume (VV), postvoid residual (PVR, measured by bladder sonography), cystometric bladder capacity, voiding efficiency (defined by the VV divided by the total bladder volume), and bladder contractility index (BCI, defined as Pdet + [5xQmax]), were measured [Figure 1].
Figure 1: Videourodynamic tracings in patients with spinal cord injury and different bladder and bladder outlet dysfunctions. (a) A patient with incomplete cervical spinal cord injury and detrusor overactivity with coordinated urethral sphincter activity; (b) a patient with complete cervical spinal cord injury and detrusor overactivity with dyssynergic sphincter activity; (c) a patient with complete thoracic spinal cord injury and detrusor overactivity with coordinated urethral sphincter activity and low bladder compliance; (d) a patient with complete thoracic spinal cord injury and detrusor overactivity with dyssynergic urethral sphincter activity; (e) a patient with complete lumbar spinal cord injury and detrusor underactivity with non-relaxing urethral sphincter activity; (f) a patient with complete sacral spinal cord injury and detrusor underactivity with contracted bladder and bilateral vesicoureteral reflux and tight bladder neck and urethral sphincterAll descriptions and terminologies used in the VUDS followed the recommendations of the International Continence Society.[10],[11] DO was defined as urodynamic evidence of spontaneous detrusor contractions occurring during bladder filling or before an uninhibited detrusor contraction voiding at bladder capacity. DU was diagnosed when female patients did not have voiding detrusor contractility of >10 cmH2O and needed to void by abdominal straining or were unable to void.[12] Male patients were identified as fulfilling the criteria for DU, defined as a BCI of <100.[13] DO-DU, known as the old terminology “detrusor hyperactivity with impaired contractility” or “DO with impaired contractility,” was assigned if the DO was associated with incomplete bladder emptying and PVR of >100 ml.[10],[12] DSD was defined as a simultaneous detrusor and urethral sphincter contraction with evidence of a neurological disorder and VUDS characteristics of an open bladder neck and narrow urethral sphincter.[10]
Bladder outlet obstruction (BOO), including BND, prostatic obstruction, high-grade cystocele, and DSD, was defined as radiographic evidence of obstruction between the bladder neck and distal urethra due to the presence of a sustained detrusor contraction of any magnitude. Male patients were diagnosed with benign prostatic obstruction if the total prostatic volume was >30 ml under transrectal ultrasound measurement in combination with features of prostatic obstruction on voiding cystourethrography (VCUG) in VUDS. To determine the presence of DSD or nonrelaxing sphincter, the urethral sphincter function assessment was performed based on the electromyographic activity and urethral sphincter appearance on VCUG during the bladder filling and voiding phases.[12]
This retrospective cross-sectional study was approved by the Institutional Review Board of the Hualien Tzu Chi Hospital (IRB: 109–107-B). All the data were anonymous before analysis. Informed consent form was waived due to the retrospective nature of the study.
Categorical and continuous variables are presented as the number of patients (proportion) and mean ± standard deviation, respectively. The occurrence of DO, DU, DSD, DO-DU, BOO, and VUR in each subgroup was compared using the Chi-squared test. Between-group variances were compared using Welch/Brown's analysis and the Games–Howell post hoc test due to the nonparametric distribution of the urodynamic parameters. A P < 0.05 indicated statistical significance. All statistical analyses were performed on a personal computer using the IBM SPSS Statistics for Windows, Version 25.0. (Armonk, NY: IBM Corp).
ResultsA total of 507 patients (388 men and 119 women) with chronic SCI and NLUTD were included in the study, including 222 (43.8%) patients with cervical SCI, 216 (42.6%) with thoracic SCI, 61 (12.0%) with lumbar SCI, and 8 (1.6%) with sacral SCI. The mean age of the patients was 44.2 ± 15.7 years, and the mean interval from diagnosis of SCI to the first VUDS was 81.8 ± 89.0 months.
The urodynamic characteristics of patients with different SCI levels are shown in [Table 1] and [Figure 2]. According to the VUDS results in all patients, 343 patients (67.7%) were diagnosed with DO, and the prevalence rate of DO was higher in patients with cervical and thoracic SCI than in patients with lumbar and sacral SCI (82.0% and 74.4% vs. 34.4% and 12.5%, P < 0.0001). A total of 132 patients (26.0%) were diagnosed with DU, and the prevalence rate of DU was 14.4% in patients with cervical SCI, 27.8% in patients with thoracic SCI, 57.4% in patients with lumbar SCI, and 62.5% in patients with sacral SCI (P < 0.0001). Similar to the DO group, the prevalence rate of DSD was also higher in patients with cervical (59.0%) and thoracic SCI (54.2%) than in patients with lumbar (34.4%) and sacral SCI (12.5%) (P < 0.0001). No statistical significance was observed in the prevalence rate of DO-DU, BOO, and VUR among patients (P = 0.917, P = 0.610, and P = 0.793, respectively).
Table 1: The videourodynamic study diagnosis among patients with spinal cord injury and different injury levels
Figure 2: The videourodynamic diagnosis among patients with spinal cord injury and different injury levels. DO: Detrusor overactivity, DU: Detrusor underactivity, DSD: Detrusor sphincter dyssynergia, AD: Autonomic dysreflexiaThe prevalence rate of DO and DSD was high in male patients with cervical (81.4% and 59.6%) and thoracic SCI (64.9% and 57.1%) and was higher than in those with the lumbar (43.5% and 43.5%) and sacral SCI (20.0% and 20.0%). Conversely, the prevalence rate of DU was lower in patients with cervical (14.8%) and thoracic SCI (28.6%) but was higher in patients with lumbar (47.8%) and sacral SCI (60.0%) (P = 0.000) [Table 2]. Similar results were also found in female patients, which showed statistically significant differences in the prevalence rates of DO, DU, and DSD (all P < 0.0001) among patients with different SCI levels [Table 2].
Table 2: The videourodynamic study diagnosis among different spinal cord injury levels in men and women[Table 3] shows the urodynamic parameter comparison among patients with different SCI levels. Bladder sensation parameters, FSF, FS, and US, were significantly lower in patients with cervical SCI than in those with lumbar SCI (P = 0.014, P = 0.015, and P = 0.008, respectively). Pdet.Qmax was significantly higher in patients with cervical and thoracic SCI than in those with lumbar SCI (P < 0.0001). In male patients with SCI, all bladder sensation parameters and Pdet. Qmax were also significantly higher in patients with cervical SCI than in those with lumbar SCI (FSF, P = 0.023; FS, P = 0.027; US, P = 0.008; Pdet.Qmax, P = 0.010) [Table 4]. In female patients, the bladder sensation parameters were not significantly different in patients with different SCI levels, whereas Pdet.Qmax was significantly higher in patients with cervical and thoracic SCI than in those with lumbar SCI (P = 0.003) [Table 4]. In addition, the BCI was significantly higher in patients with thoracic SCI than in those with lumbar SCI (P = 0.038).
Table 3: Urodynamic variables comparison among groups of different spinal cord injury levels in overall patients
Table 4: Urodynamic variables comparison among groups of different spinal cord injury levels in men and womenBladder management among patients with different SCI levels is shown in [Supplement Table 1]. Clean intermittent self-catheterization was the most common bladder management among all patients (50.5%). More patients with cervical SCI (24.3%) chose suprapubic cystostomy for bladder emptying than those with thoracic (T1–T6, 7.6%; T7–T12, 13.3%) or lumbar SCI (18.0%) (P = 0.008). Patients with cervical SCI who received external sphincterotomy (10.4%) or transurethral incision of the bladder neck (15.3%) were significantly higher than those with thoracic or lumbar SCI levels (P < 0.0001 and P = 0.004, respectively).
DiscussionThis study aimed to analyze the differences in VUDS findings in patients with different SCI levels, which may help in the clinical decision-making of bladder management. A high prevalence of NLUTD was found in patients with chronic SCI, including DO and DSD in patients with suprasacral lesions and DU in patients with lumbosacral lesions.
NLUTD commonly occurs among patients with SCI. Normal micturition requires coordination of a neuronal circuit between the brain, spinal cord, urinary bladder, and urethra. The sacral micturition center (located at S2–S4), pontine micturition center, and cerebral cortex are responsible for facilitating and inhibiting micturition. Parasympathetic efferent from the sacral cord at S2–S4 via the pelvic nerves provides excitatory input to the bladder. Bladder contraction results from muscarinic receptor stimulation. The external sphincter is inhibited through the somatic nerves via the pudendal nerve. The sympathetic efferent originates from the intermediolateral gray column T11–L2 and supplies the bladder and urethra. These nerves provide inhibitory input to the bladder through the hypogastric nerve. Sympathetic stimulation causes bladder relaxation through beta-receptor stimulation and sphincter contraction through alpha-receptor stimulation.[14] Following the spinal shock associated with SCI above S1, reflex bladder function will occur. The consciousness of bladder filling might not be totally absent. However, voluntary inhibition of the micturition reflex is lost. Typical urodynamic findings of SCI include DO and DSD. Patients with SCI may have both urinary incontinence due to DO in the storage phase and voiding difficulty due to DSD. Discoordinated urethral sphincter contraction during the voiding phase results in high voiding pressure and large PVR, resulting in recurrent UTI, upper urinary tract deterioration, and renal failure if not properly treated.[15],[16]
Kaplan et al. studied the SCI levels and urodynamic findings of 489 patients.[17] Of all patients with cervical lesions, 85% had mainly neurogenic detrusor overactivity (NDO) and DSD. Furthermore, patients with thoracic SCI had NDO, with 90% also having DSD. Patients with a lumbar SCI had the least predictable urodynamic pattern, where 30% of patients had NDO, and 30% had both NDO and DSD. Chen et al. conducted a study of 28 cross-national SCI surveys in Taiwan and reported high NDO and DSD rates in patients with cervical SCI (82.1% and 60.0%, respectively) and thoracic SCI (55.8% and 32.5%, respectively).[18] In this study, DO and DSD were observed in 67.7% and 53.3% of all patients with SCI who were referred for NLUTD management, respectively. In addition, about 78.2% of patients with NDO were also diagnosed with DSD.
The sacral parasympathetic nucleus, which controls bladder emptying, and Onuf's nucleus, which excites the external urethral sphincter, can be damaged in patients with sacral SCI, resulting in DU with high or normal bladder compliance and a loss of normal bladder sensation. Patients with sacral SCI have a low risk of upper tract deterioration than those with suprasacral SCI due to the initial low intravesical pressure. However, patients with sacral SCI can also develop decreased bladder compliance from neurologic decentralization.[19] Therefore, these patients should be closely monitored with regular urodynamic testing. In this study, 132 patients (26%) presented with DU after SCI, which was predominantly observed in patients with lumbar and sacral SCI (57.4% and 62.5%, respectively). Furthermore, some patients with cervical SCI or thoracic SCI presented with DU (14.4% and 27.8%, respectively); among them, 7.6% had low bladder compliance (<20 cmH2O). Chen et al. and Kooshesh et al. reproted that 26.0% and 45.5% of patients with suprasacral lesions presented with DU.[18],[20] Arnold et al.[21] reported two cases of upper motor neuron lesions, presumably due to a coexistent clinical or subclinical sacral spinal cord lesion. In this study, we also observed that seven patients (1.4%) had DO-DU, indicating that some patients with SCI with DO also have low detrusor contractility.
In this study, BND was observed in 25% of patients, which was not statistically significant among different patient groups. Krongrad and Sotolongo. reported that the incidence of neurogenic BND was similar to that of DSD. The incidence of DSD was highest in patients with high thoracic SCI (67%), followed by those with low thoracic SCI (56%), those with cervical SCI (43%), and finally those with lumbar SCI (20%). The incidence of BND was also highest in patients with high thoracic SCI (27%), followed by those with low thoracic SCI (22%) and those with cervical SCI (7%). No BND was observed in patients with lumbar SCI.[22] The influence of sympathetic and pudendal nerve hyperactivity on the detrusor nucleus in the sacral cords may be enhanced after suprasacral SCI, thereby inducing bladder dysfunction and DSD. Moreover, BND causes BOO in patients with high thoracic or cervical SCI. BND is usually associated with DSD at a high suprasacral SCI level. Therefore, it may represent a more severe form of sympathetic hyperactivity. Patients with SCI and BND have a delayed opening of the bladder neck at the start of micturition. Therefore, patients may have prolonged autonomic dysreflexia (AD) and more difficulty urinating. Furthermore, the PVR increases, and patients need an α-adrenergic blocker to relieve their AD symptoms. Thus, early BND identification is important to prevent further urologic complications, such as UTI or upper urinary tract exacerbation.[23]
In this study, VUR was observed in 9.9% of patients, and no significant difference was observed between different SCI levels (P = 0.793). Hackler et al. demonstrated that VUR occurs in more than 29% of patients with neurogenic bladder. This condition is more common when the lesion is at the suprasacral level. Long-term high detrusor pressure and high-grade VUR are responsible for renal damage and failure.[24] Schöps et al. reported that VUR was quite rare (5%) and generally low grade in patients with SCI. The discrepancy in the incidence of VUR in different SCI surveys might result from active initial bladder management and pharmacological treatment in the early stage of SCI. Thus, regular follow-up of bladder storage and voiding function with urodynamic investigation allows for patient-tailored bladder management.[25]
Bladder sensation parameters, including FSF, FS, and US, were significantly lower in patients with cervical SCI than in those with lumbar SCI. Bladder sensation was usually lower in patients with lumbar SCI than in those with cervical SCI. Ersoz et al. reported that the presence of bladder filling sensation in many patients with SCI revealed the potential for sensation-dependent bladder emptying in patients with SCI, particularly in those with complete SCI lesions below T10 and with incomplete SCI lesions. Preserving bladder sensation may prevent early emptying attempts, unnecessary catheterizations, and bladder overdistension episodes and may improve the patient's self-esteem and quality of life.[26]
This study has some limitations. First, this was a retrospective study, which may have resulted in patient selection bias. Second, patients were investigated at different time points after the initial bladder management for SCI with NLUTD, and urodynamic parameters are potentially biased by different investigation time points. Third, only a small number of patients had sacral SCI. This small number of patients may affect the statistical power. Finally, this study did not use the American Spinal Injury Association (ASIA) Impairment Scale classification to evaluate patients with complete or incomplete lesions. Therefore, the choice of bladder management and surgical procedure cannot be compared based on the ASIA classification.
ConclusionThe VUDS of NLUTD revealed a high prevalence of DO, DU, and DSD, which varied among patients with different SCI levels. Patients received different surgical or medical treatments based on their VUDS findings. A VUDS is necessary for patients with SCI and NLUTD and is helpful in the decision-making of bladder management.
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Conflicts of interest
Prof. Hann-Chorng Kuo, an editorial board member at Urological Science, had no role in the peer review process of or decision to publish this article. The other author declared no conflicts of interest in writing this paper.
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