Abstract
Context
Individuals with suprasacral spinal cord injury (SCI) often face significant clinical and quality-of-life (QoL) burdens due to neurogenic detrusor overactivity (NDO). Transcutaneous tibial nerve stimulation (TTNS) is a non-invasive neuromodulation technique that may serve as a treatment option, but evidence regarding its effectiveness in anticholinergic-refractory NDO remains limited.
Objectives
To evaluate the effectiveness of TTNS on urodynamic parameters in individuals with SCI who have anticholinergic-refractory NDO.
Methods
Twenty-one patients with suprasacral SCI completed the study, of whom 42.9% had complete injuries. Twelve TTNS sessions (20 Hz, 200 ms, 30 minutes) were administered twice weekly. Urodynamic outcomes were assessed using reflex volume (RV), maximal cystometric capacity (MCC), maximal detrusor pressure (Pdet-max), and bladder compliance (BC). TTNS was considered positive if RV and/or MCC increased by ≥100 mL or ≥50% from baseline. The Neurogenic Bladder Symptom Score (NBSS) was used to assess symptom severity.
Results
Significant improvements were observed in RV, MCC, Pdet-max, and BC after TTNS (P < 0.001). No statistically significant differences in urodynamic parameter changes following TTNS were observed between groups categorized by either injury severity or duration (P > 0.05). TTNS was considered positive in 9 patients (42.9%) based on RV and/or MCC improvements. Following TTNS, significant improvements were observed in the incontinence, storage and voiding, QoL subdomains of the NBSS (P < 0.05).
Conclusion
Although Pdet-max remained >40 cmH2O in nearly half of the patients after TTNS, improvements in both urodynamic parameters and NBSS scores indicate that TTNS may provide clinical benefit in patients with anticholinergic-refractory NDO.
KEYWORDS: Neurogenic bladder, Transcutaneous Tibial nerve stimulation, Spinal cord injury, Urodynamics, Detrusor overactivity
Introduction
Neurogenic detrusor overactivity (NDO) causes considerable clinical challenges and negatively affects the quality of life (QoL) in individuals with suprasacral spinal cord injury (SCI). NDO leads to high intravesical pressures, increasing the risk of upper urinary tract damage and potential renal failure. It can also result in urinary incontinence, which often limits social participation and daily activities (1). Accordingly, the primary goal of NDO treatment is to protect the upper urinary tract by controlling high bladder pressures and to enhance QoL by reducing incontinence (2). The current gold standard treatment for NDO in individuals with SCI includes clean intermittent catheterization combined with anticholinergic medications. However, anticholinergic drugs may be ineffective in adequately controlling bladder pressure in some patients, even at high doses. On the other hand, anticholinergic drugs cannot be prescribed in adequate doses in some patients due to side effects (i.e. dry mouth, sedation, constipation, etc.) (3). Additionally, the long-term effects of anticholinergic treatment remain unclear, and new evidence suggests a risk of dementia with high cumulative doses of anticholinergic medications (4).
Invasive procedures such as intravesical botulinum toxin injections or major surgical interventions are considered for the management of NDO when pharmacological treatments fail. Although onabotulinum toxin A injection is effective for NDO in patients with SCI, its application has several limitations (e.g. high cost, the requirement for invasive cystoscopy, the need for repeated annual treatments, and potential adverse events such as urinary tract infections and hematuria). Moreover, while the effect of onabotulinum toxin A may last up to 9 months, its efficacy can diminish with repeated injections (5). Another option for refractory cases is major surgical procedures such as augmentation cystoplasty. Although augmentation cystoplasty provides good long-term outcomes, it is associated with complications that may lead to significant morbidity (6).
Neuromodulation, which modulates activity in one neural pathway through synaptic interaction with another neural pathway, is a treatment option for detrusor overactivity. The complex array of neural interactions involving descending control and spinal reflexes presents several potential targets for neuromodulation (7). Tibial nerve stimulation (TNS), initially described by McGuire et al. in 1983 (8), is an FDA-approved technique used to suppress detrusor overactivity. The tibial nerve originates from the L4–S3 nerve roots, and the detrusor muscle receives its innervation primarily from S2–S3, making this pathway a rational target for modulation. Stimulation of the tibial nerve leads to retrograde neuromodulation of the sacral spinal cord by activating afferent fibers, thereby reducing detrusor overactivity and alleviating symptoms such as urinary frequency and urgency. TNS is primarily administered through percutaneous tibial nerve stimulation (PTNS), where a 34-gauge needle electrode is inserted approximately 4–5 cm superior to the medial malleolus to activate the tibial nerve (9). Systematic reviews and meta-analyses have demonstrated that PTNS offers efficacy comparable to that of anticholinergic medications, with only mild side effects such as minor bleeding, local discomfort, or skin irritation at the needle insertion site (10). As a non-invasive alternative to PTNS, transcutaneous tibial nerve stimulation (TTNS) uses surface electrodes to stimulate the tibial nerve. Recent studies suggest that TTNS provides therapeutic benefits similar to PTNS in the management of detrusor overactivity (11).
Most studies on TNS in the literature investigate on non-neurogenic detrusor overactivity, and TNS is primarily used in clinical practice for patients with idiopathic detrusor overactivity (12). There are limited studies on the efficacy of TNS in NDO, and these are often studies with small sample sizes and heterogeneous patient populations (13). A few studies have demonstrated that TNS improves cystometric capacity and detrusor pressure in patients with SCI (14,15). Nevertheless, limited evidence exists regarding the effectiveness of TNS in patients with anticholinergic-refractory NDO. Therefore, this study aimed to evaluate the effectiveness of TTNS on urodynamic parameters in individuals with suprasacral SCI who have anticholinergic-refractory NDO. Additionally, we aimed to assess the impact of TTNS on the severity of symptoms associated with NDO.
Methods
From November 2023 to July 2024, individuals with suprasacral SCI who were hospitalized in the SCI rehabilitation clinic of the tertiary hospital were included in the study. A total of 49 patients were assessed, and 28 met the inclusion criteria. After two patients declined to participate, 26 were enrolled in the study. Of these, two patients were discharged before completing the study, and two were excluded due to the development of urinary tract infection. One patient withdrew, reporting a worsening of urinary incontinence with TTNS. Ultimately, 21 patients completed the study. All procedures performed in this study involving human participants were in accordance with the Declaration of Helsinki. This study was approved by the ethical committee of our hospital (protocol no. E2-22-2030), and written informed consent was obtained from all participants prior to enrollment.
Inclusion criteria for the study were as follows: (a) individuals aged ≥18 years with suprasacral SCI; (b) presence of NDO confirmed by urodynamics (NDO characterized by spontaneous or provoked involuntary detrusor contractions during the filling phase); (c) use of anticholinergic medication at a stable dose for at least three months prior to the initial urodynamic assessment; (d) a maximum detrusor pressure >40 cmH2O during the filling phase of urodynamics or complaints of urinary incontinence between intermittent catheterizations. Exclusion criteria included the presence of other diseases that could affect lower urinary tract function (e.g. polyneuropathy, Parkinson’s disease), other genitourinary conditions (e.g. benign prostatic hyperplasia, pelvic floor dysfunction, bladder stones), or symptomatic urinary tract infection. Additional exclusion criteria were the administration of onabotulinumtoxinA within the previous six months and/or a history of lower urinary tract surgery.
The demographic characteristics of the participants and the level/severity of SCI according to the “American Spinal Cord Injury International Standards for Neurological Classification of SCI” were recorded (16).
Transcutaneous tibial nerve stimulation (TTNS)
Two adhesive surface electrodes were placed according to the protocol of Chen et al. (14). The negative electrode was placed just behind the right medial malleolus, and the positive electrode was placed 10 cm above the negative electrode along the tibial nerve. The correct positioning of the negative electrode was verified by observing either flexion of the hallux or fanning of the toes in response to increasing current intensity. Stimulation was delivered at a frequency of 20 Hz with a pulse width of 200 μs in continuous mode. The intensity was gradually increased to the maximum tolerable level – avoiding lower limb muscle spasms in patients with complete SCI and avoiding discomfort at the stimulation site in patients with incomplete SCI. TTNS was administered twice weekly for a total of 12 sessions, each lasting 30 minutes. All participants continued their anticholinergic medications at the same dosage as prior to enrollment in the study.
Urodynamic evaluation and outcome measures
The Libra + (MMS, Enschede, The Netherlands) urodynamic measurement system was used for urodynamic evaluation. Cystometry was performed at 20 ml/min filling rate with room temperature sterile saline. Urodynamic terminology was used in accordance with the definitions of the International Continence Society (ICS) (17). Reflex volume (RV) was defined as the bladder filling volume at which the first involuntary detrusor contraction occurred. Maximal cystometric capacity (MCC) was determined as the volume at which the patient reported a strong desire to void, experienced discomfort, or urinary leakage occurred, thereby terminating the filling phase. Maximal detrusor pressure (Pdet-max) was recorded as the highest detrusor pressure observed during bladder filling. Bladder compliance (BC) was calculated by dividing the change in bladder volume by the corresponding change in detrusor pressure during filling (17). Although there is no clear consensus on urodynamic parameters, safety cut-off values have been defined based on the relevant literature to prevent upper urinary tract complications associated with NDO. MCC <300 mL, Pdet-max >40 cmH2O, and BC <10 mL/cmH2O were considered indicative of a higher risk for upper urinary tract deterioration, and urodynamic parameters were categorized accordingly (18,19). The TTNS effect was considered positive if RV and/or MCC increased by 100 ml and/or 50% after TTNS compared to before (20).
Assessment of neurogenic bladder symptoms
Neurogenic Bladder Symptom Score (NBSS) was used to evaluate the severity of neurogenic bladder symptoms (21). The Turkish validity and reliability study of the NBSS was conducted by Güler et al. (22). The NBSS is a 24-item questionnaire, with items rated on a Likert scale consisting of 4 or 5 ordinal response options. It assesses bladder symptoms across three domains: incontinence (scored 0–29), storage and voiding (scored 0–22), and consequences (scored 0–23). In addition, there is a single general urinary QOL question, scored from 0 (pleased) to 4 (unhappy). For all domains, higher scores indicate a worse symptom burden or poorer QOL. Additionally, the Visual Analog Scale (VAS) (0–10) was used to assess discomfort associated with TTNS, where 0 indicated no discomfort and 10 represented the most severe discomfort experienced.
Statistical analysis
All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) version 15.0 (SPSS Inc., Chicago, IL). Continuous variables were presented as median (minimum – maximum), and categorical variables as frequencies and percentages. The conformity of the data to the normal distribution was examined using the Kolmogorov–Smirnov test. The paired t-test was used to compare mean values of urodynamic parameters before and after TTNS, and the Wilcoxon signed-rank test was used to compare median NBSS scores. Categorical variables before and after TTNS were compared using the McNemar test. The Mann – Whitney U test was used to compare changes in urodynamic parameters with TTNS between groups based on injury severity (complete vs. incomplete) and injury duration (≤6 months vs. > 6 months). P value of <0.05 was considered statistically significant. Sample size was determined by an a priori power analysis using the G*Power software, assuming an α level of 0.05 and a power of 80%.
Results
Of the 21 patients included in the study, 13 (61.9%) were male, and the mean age was 32.9 ± 12.2 years (range: 19–61). The mean duration of injury was 233.3 ± 86.6 days (range: 120–360), with 12 patients (57.1%) having an injury duration > 6 months. Complete SCI was present in 9 patients (42.9%). Patient characteristics are summarized in Table 1.
Table 1.
Demographic and clinical characteristics of the participants.
| n = 21 | |
|---|---|
| Age, year (mean ± SD) | 32.9 ± 12.2 |
| Sex, n (%) | |
| Male | 13 (61.9) |
| Female | 8 (38.1) |
| Injury duration, day (mean ± SD) | 233.3 ± 86.6 |
| ≤ 6 months, n(%) | 9 (42.9) |
| >6 months | 12 (57.1) |
| Completeness of SCI, n(%) | |
| Complete (AIS A) | 9 (42.9) |
| Incomplete (AIS B-D) | 12 (57.1) |
| Level of SCI, n(%) | |
| Tetraplegia | 5 (23.8) |
| Paraplegia | 16 (76.2) |
| Medications for detrusor overactivity, n(%) | |
| Oxybutynin | 7 (33.3) |
| Trospium | 9 (42.9) |
| Tolterodine | 3(14.3) |
| Oxybutynin + Propiverine | 1 (4.8) |
| Trospium + Mirabegron | 1 (4.8) |
SCI, Spinal cord injury, AIS, American Spinal Injury Association Impairment Scale.
Post-TTNS assessments showed significant improvements in RV and MCC compared to baseline values (P < 0.001). Additionally, Pdet-max was significantly reduced and BC was significantly increased after TTNS (P < 0.001) (Table 2). After TTNS, a mean increase of 72.1 ± 72.9 ml in RV and 71.1 ± 51.6 ml in MCC was observed. The mean decrease in Pdet-max was 16.2 ± 11.9 cmH2O. No statistically significant differences in urodynamic parameter changes following TTNS were observed between groups categorized by either injury severity (complete vs. incomplete) or injury duration (≤6 months vs. > 6 months) (P > 0.05).
Table 2.
Comparison of urodynamic parameters before and after TTNS.
| Pre-TTNS | Post-TTNS | P* | |
|---|---|---|---|
| RV, ml | 158.6 ± 85.1 | 230.7 ± 108.1 | <0.001 |
| MCC, ml | 266.1 ± 123.2 | 337.1 ± 132.7 | <0.001 |
| Pdet (max), cmH2O | 63 ± 26.3 | 46.8 ± 23.2 | <0.001 |
| BC, ml/ cmH2O | 5.6 ± 4.3 | 9.4 ± 5.8 | <0.001 |
TTNS, Transcutaneous tibial nerve stimulation; RV, Reflex volume; MCC, Maximal cystometric capacity; Pdet(max), Maximal detrusor pressure at filling cystometry; BC, Bladder compliance, *P < 0.05: significant.
The rates of MCC <300 ml, BC <10 ml/cmH2O, and Pdet-max >40 cmH2O were significantly reduced after TTNS compared to before TTNS (P < 0.05) (Figure 1). The effect of TTNS was considered positive in 9 patients (42.9%) based on improvements in RV and MCC.
Figure 1.
Comparison of Group Rates Based on Safety Cut-off Values in Urodynamic Parameters Pre- and Post-TTNS. TTNS: Transcutaneous tibial nerve stimulation, RV: Reflex volume, MCC: Maximal cystometric capacity, Pdet(max): Maximal detrusor pressure at filling cystometry, BC: Bladder compliance. P1(Comparison of pre-TTNS and post-TTNS MCC <300 ml rates): 0.008; P2 (Comparison of pre-TTNS and post-TTNS Pdet (max) > 40 cmH2O rates): 0.031; P3 (Comparison of pre-TTNS and post-TTNS BC <10 ml/cmH2O rates): 0.016. *P < 0.05: significant
Despite TTNS, Pdet-max remained >40 cmH2O in 47.6% of patients, and intravesical botulinum toxin injections were subsequently required in 7 patients (33.3%).
Following TTNS, significant improvements were observed in the incontinence, storage and voiding, QoL subdomains of the NBSS (P < 0.05); however, no significant change was detected in the consequences subdomain (P = 0.083) (Table 3). One patient withdrew from the study due to an increase in urinary incontinence with TTNS. The mean VAS-Discomfort score reported by participants was 2.6 ± 0.9.
Table 3.
Comparison of NBSS before and after TTNS.
| Domains | Pre-TTNS Median (min–max) |
Post-TTNS Median (min–max) |
P* |
|---|---|---|---|
| Incontinence (0–29) | 19 (14–29) | 12 (8–25) | <0.001 |
| Storage and voiding (0–22) | 17 (9–19) | 13 (4–18) | <0.001 |
| Consequences (0–23) | 10 (7–19) | 10 (7–18) | 0.083 |
| NBSS QoL question (0–4) | 3 (2–4) | 2 (0–4) | <0.001 |
NBSS, Neurogenic Bladder Symptom Score; TTNS, Transcutaneous tibial nerve stimulation; QoL, Quality of life. *P < 0.05: significant.
Discussion
After TTNS, significant improvements were observed in RV, MCC, Pdet-max, and BC compared to baseline in patients with SCI who had anticholinergic-refractory NDO. No significant differences in TTNS-related changes were found between groups categorized by injury severity or duration. The TTNS response was considered positive in 42.9% of patients based on improvements in RV and/or MCC. Furthermore, significant improvements were observed in the incontinence, storage and voiding, and QoL subdomains of the NBSS.
In patients with suprasacral spinal cord injury (SCI), the loss of supraspinal control leads to involuntary reflexive bladder contractions and impaired coordination between the detrusor and urethral sphincter. This dysfunction can result in elevated intravesical pressure, potentially causing structural bladder damage, vesicoureteral reflux, and renal insufficiency. Anticholinergic medications are considered the first-line treatment for NDO associated with SCI. However, side effects of these drugs can negatively impact treatment adherence in some patients (2). Co-administration of TTNS with anticholinergics may provide an opportunity to reduce the dose and side effects of the drugs. On the other hand, anticholinergic therapy may be inadequate to control NDO-related symptoms and urodynamic parameters (high detrusor pressure, low bladder capacity, low BC, etc.) in some individuals with SCI (3). In such cases, alternative treatment modalities like TNS may be considered before progressing to more invasive or surgical interventions.
Several studies in the literature have investigated the acute effects of transcutaneous TTNS on urodynamic parameters. In a study with 44 participants, 15 of whom had SCI, cystometry was performed during TTNS. Similar to our study, a positive TTNS response was defined as an increase of ≥100 mL in RV and/or ≥50% in MCC compared to baseline measurements. The authors reported a significant increase in cystometric volumes during stimulation and classified 50% of the participants as responders to TTNS (20). In our study, a cumulative positive response rate of 42.9% in cystometric volumes was observed after 12 TTNS sessions in patients with SCI and anticholinergic-resistant NDO. Kamboonlert K et al. (23) also evaluated the acute effects of bilateral TTNS on urodynamic parameters in individuals with SCI. Their findings showed that bilateral TTNS was more effective than sham stimulation in improving RV, MCC, BC. Furthermore, they noted that its efficacy was comparable to that of anticholinergic treatment.
In most studies, TNS is usually administered once or twice weekly for a total of 10–12 sessions. Some reports suggest that the treatment effect is associated with the total number of stimulations rather than the duration of the treatment period (13). Chen et al. (14) applied TTS twice weekly in patients with SCI who were not receiving oral therapy to inhibit DO. They reported significant improvements in all bladder diary parameters (e.g. volume per catheterization and daily leakage volume) and QoL at both 2 and 4 weeks after stimulation, with no significant difference between the two time points. In another study, 16 participants with SCI applied TTNS at home for 30 minutes daily over 4 weeks. Among those using anticholinergic medications, 86% had dose reductions, which led to fewer drug-related side effects and improved QoL (24).
There are limited studies evaluating the effectiveness of TTNS in individuals with SCI who have anticholinergic-refractory NDO. Andrews and Reynard (15) examined the impact of TNS in a patient with SCI and inadequate response to anticholinergic therapy who was scheduled for augmentation cystoplasty. They applied PTNS (25 Hz, 250 µs, 30 mA) during urodynamics and observed an increase in MCC from 150 mL to 315 mL. In another study, PTNS (20 Hz, 200 µs, 30 minutes once weekly for 12 weeks) was evaluated in women with idiopathic DO resistant to both first – and second-line treatments. Significant improvements were reported in detrusor overactivity symptoms (daily micturition frequency, urgency, urgency incontinence) and quality of life (25). Yildiz and Celtek (26) assessed the effect of TTNS in women with idiopathic DO resistant to pharmacologic agents, comparing outcomes with a control group that was pharmacologically naïve. Both groups showed significant improvements in incontinence severity, frequency of incontinence episodes, symptom severity, treatment satisfaction, and QoL. However, the improvements were more pronounced in the pharmacologically naive group.
In our study, one patient discontinued participation due to worsening urinary incontinence with TTNS. On the other hand, significant improvements were observed in the incontinence, storage and voiding, and QoL subdomains of the NBSS. However, no significant change was detected in the consequences subdomain. One possible explanation may be the short follow-up period of the study. Another possibility is that this subdomain includes items evaluating conditions that were either part of the study’s exclusion criteria or associated with the anticholinergic medications used by all participants. TTNS is a noninvasive and more accessible neuromodulation neuromodulation technique (11,14). Moreover, the overall mean VAS-Discomfort score in our study was 2.6 ± 0.9, indicating that the intervention was well tolerated.
While our study has some limitations, we believe it makes a meaningful contribution to the understanding of non-invasive neuromodulation methods for the management of NDO in patients with SCI. The most significant limitation is the absence of a sham control group Since the study focused on urodynamic outcomes requiring invasive testing, we did not consider it ethically appropriate to perform urodynamic assessments following sham stimulation. Another limitation is the relatively small sample size, which limited our ability to explore subgroup differences based on injury severity and duration. We believe that future studies with larger sample sizes will be essential to evaluate the potential influence of both injury duration and severity on the effectiveness of TTNS.
Conclusion
TTNS is a non-invasive and safe neuromodulation method that can be administered at home, making it a more accessible option for long-term management in patients with NDO. In our study, although Pdet-max remained >40 cmH2O in nearly half of the patients after TTNS, improvements in both urodynamic parameters and NBSS scores indicate that TTNS may provide clinical benefit in patients with anticholinergic-refractory NDO. TTNS may serve as a supportive treatment strategy to enhance the effects of anticholinergic medications or to reduce their dosage due to potential side effects. We believe that further studies with larger sample sizes could contribute to expanding the clinical use of TTNS in the management of NDO among individuals with SCI.
Disclaimer statements
Funding: None.
Declaration of interest: None.
Conflicts of interest: There is no conflict of interest.
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