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Background:
Systematic Review

Relevance of Leg Rehabilitation to Modulating Neurogenic Lower Urinary Tract Symptoms: A Systematic Review

by
Gianluca Ciardi
1,2,
Donatella Giraudo
3,
Milena Fontana
2,
Chiara Citterio
1,
Paola Gandolfi
1 and
Gianfranco Lamberti
1,2,*
1
Department of Rehabilitative Medicine, Azienda Usl Piacenza, Fiorenzuola d’Arda Hospital, Via Roma 29, 29017 Fiorenzuola d’Arda, Italy
2
Physiotherapy Degree Course, Department of Medicine and Surgery, University of Parma, Piacenza Training Centre, Viale Abruzzo 12 B/C, 29017 Fiorenzuola d’Arda, Italy
3
Department of Urology, San Raffaele Turro Hospital, Via Stamira D’Ancona, 20, 20127 Milano, Italy
*
Author to whom correspondence should be addressed.
Bioengineering 2025, 12(2), 127; https://doi.org/10.3390/bioengineering12020127
Submission received: 30 November 2024 / Revised: 20 January 2025 / Accepted: 25 January 2025 / Published: 29 January 2025
(This article belongs to the Special Issue Advances in Physical Therapy and Rehabilitation)
Browse Figure
Versions Notes

Abstract

:
Neurogenic lower urinary tract dysfunction (NLUTD) is a secondary complication of a wide range of neurological disorders, which affects patients’ everyday life and self-efficacy. Some brain imaging studies have shown an overlap between motor activation of the pelvic floor and lower limbs. This systematic review sought to examine the possibility of improving overactive bladder outcomes through a conservative approach based on lower limb training. We conducted a systematic literature review, following the PRISMA guidelines. The following databases were searched: PEDro, PubMed, TRIP, Cochrane Library, EDS base index, Google Scholar, and CINAHL. The PEDro Scale and Cochrane Risk of Bias Assessment Tool were used to assess the overall study quality and sources of bias. A total of 5567 records were retrieved through the systematic search, of which 104 were sought for retrieval; two cohort studies and one randomized controlled trial were finally included. Urodynamics and specific bladder functionality questionnaires showed preliminary evidence of improvement following lower limb stimulation, implemented according to different treatment types (exoskeleton training and weight-suspension walking training). Lower limb-focused exercises showed promising results for improving bladder function, despite the small number of studies and small sample sizes. Future research should confirm this hypothesis using larger samples.

1. Introduction

Neurogenic lower urinary tract dysfunction (NLUTD) encompasses a spectrum of urinary disorders resulting from abnormal nervous system control of the bladder [1,2,3]. This condition significantly affects individuals with a variety of neurological impairments other than spinal cord injury (SCI) [4], including multiple sclerosis, Parkinson’s disease, diabetes-induced neuropathy, and other conditions that lead to various degrees of bladder dysfunction [5]. The broad relationship between NLUTD and neurological disorders highlights the complexity of managing affected individuals, as the type and extent of bladder dysfunction of the lower urinary tract, secondary to neurological pathology, varies depending on the site of the lesion, its extent, and the progression of the neurological disease [6]. Symptomatic expression of NLUTD has been hypothesized to be the result of several pathophysiological factors, including modifications of the urethra/urothelium, urinary microbiota, and hormonal/gastrointestinal dysfunctions [7]. Classification schemes for lower urinary tract dysfunction have been proposed [8,9] as follows: suprapontine lesions, which typically present with urinary incontinence secondary to detrusor overactivity, with normal bladder-sphincter synergy [10]; suprasacral lesions, often characterized by bladder-sphincter dyssynergy with urinary incontinence and concurrent partial retention [11]; and sacral lesions with compromised detrusor function and sphincter and pelvic floor muscle paralysis [12]. In suprapontine lesions, lower urinary tract dysfunction may be due to, or strongly influenced by, motor and cognitive dysfunctions, which can cause functional urinary incontinence [13].
In the management of bladder disorders in patients with neurological conditions, a comprehensive clinical assessment, incorporating a thorough integration of clinical data, urodynamic findings, and imaging results, and the formulation of a tailored rehabilitation program are crucial. The initial step of this evaluation involves detailed anamnesis, including gathering information on the onset, history, precipitating factors, frequency and severity of episodes, pharmacological treatments, colonic inertia, and comorbid conditions, such as obesity, diabetes, and previous perineal dysfunction, particularly in female patients [14,15]. Recently, the adoption of quantitative instruments has enhanced the precision of symptom evaluation. Notably, a 36-h bladder diary [16] offers insights into fluid intake and output balance, voiding frequency, and characteristics of incontinence. Furthermore, disease-specific validated scales can quantify the impact of urinary symptoms on patients’ quality of life [17,18]. The subsequent phase entailed a physical examination to identify contributing factors and assess high-risk comorbidities. This includes the evaluation of sacral area sensitivity, anal tone, pelvic sensation, and the bulbocavernosus and anal reflexes [1,12]. Ultimately, urodynamic testing provides a detailed analysis of the mechanism of incontinence and the potential risk of urinary tract damage, warranting periodic assessments to inform patient management effectively [19,20,21,22].
The therapeutic landscape for NLUTD is extensive and encompasses a range of pharmacological and non-pharmacological interventions. Pharmacologically, antimuscarinics and beta-3 adrenoceptor agonists are frequently employed to manage detrusor overactivity by reducing bladder muscle contractions [23,24,25]. For more severe cases, intradetrusor injections of botulinum toxin have demonstrated efficacy in decreasing incontinence episodes by blocking the release of acetylcholine at the neuromuscular junction, decreasing detrusor contractility [26,27].
Beyond pharmacotherapy, neuromodulation techniques have been recognized to have potential for restoring bladder control by directly modulating the neural pathways involved in bladder dysfunction [28,29]. Sacral neuromodulation [30,31] involves electrical stimulation of the sacral nerve roots to restore normal bladder activity, whereas percutaneous tibial nerve stimulation (PTNS) uses electrical impulses delivered to the tibial nerve, leveraging its somatic afferent inputs to influence neural control of the bladder. These approaches offer a less invasive alternative and have yielded promising outcomes.
Exercise can also be considered a neuromodulatory strategy, and its positive effects on neuronal plasticity in cases of disability resulting from neurological diseases are well-known [32]. Similarly, the efficacy of pelvic floor therapeutic exercises has been demonstrated in lower urinary tract disorders after stroke and in cases of multiple sclerosis [33,34,35,36,37,38].
In a cohort of healthy men, a previous study showed that pelvic floor activity activated cortical regions associated with lower extremity movement, suggesting an overlap in the brain areas controlling pelvic functions and those controlling leg movement [39]; in addition, integration seems extended to spinal circuits, as suggested by post-SCI restoration animal models [40]. This finding aligned with those of earlier brain imaging studies, which indicated that stimuli from leg movements could inhibit overactive bladder symptoms, thereby supporting the concept of peripheral neuromodulation. Considering the evidence of an overlap of the motor control areas of the pelvic floor and that of the lower limbs in the brain, it could be hypothesized that it would be possible to achieve a similar control effect secondary to exercises proposed for the lower limbs.
The rationale behind considering lower limb exercise as a neuromodulatory strategy for detrusor overactivity lies in the potential of such physical activity to influence bladder control via neural plasticity. Regular, targeted exercise may not only enhance general health but may also exert a specific modulatory effect on bladder function by engaging the neural mechanisms shared between lower limb and pelvic floor activities.
Despite the extensive neurophysiological background supporting the role of lower limb exercise in the modulation of NLUTD [41,42,43], no systematic review to date has definitively addressed the topic. There is, therefore, a knowledge gap, both in terms of the exercise modalities to be proposed and their administration in terms of timing and frequency of intervention.
By synthesizing current research findings and integrating insights from neurophysiology and rehabilitation science, in this systematic literature review, we evaluated whether lower limb-based exercise, as a viable, non-pharmacological intervention, can suppress detrusor overactivity through a neuromodulatory effect to manage NLUTD across a wide range of neurological conditions. This investigation will not only contribute to a deeper understanding of NLUTD pathophysiology but also open new avenues for innovative, patient-centered therapeutic strategies.

2. Materials and Methods

This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis for Network Meta-analysis (PRISMA-NMA) [44] guidelines and the Cochrane Handbook for Systematic Reviews of Interventions. The search protocol was registered on INPLASY under number 202270099 (https://inplasy.com/inplasy-2022-7-0099/, 29 November 2024) [45].
Our research questions (RQs) were as follows:
  • RQ1: Is there a relationship between lower limb-centered rehabilitation and the inhibition of NLUTD?
  • RQ2: Could a specific rehabilitation program be useful to better manage neurological bladder dysfunction?

2.1. Search Strategy

PubMed (Medline), the Cochrane Database, Google Scholar, PEDro, the Trip database, the EDS base index, CINAHL, Web of Science, and Scopus databases were systematically searched for English-language articles published from 2018 to 28 February 2024, following the strategy depicted in Supplementary Material S1.
Articles were considered eligible if they agreed with the items defined by the following PICO model:
  • (P) Participants: Patients with neurological conditions, with a diagnosis of NLUTD
  • (I) Intervention: Lower limb exercises focused on controlling NLUTD (hypothesized interventions: leg strength/stretching, exercises, therapeutic walking with braces, and exoskeleton training)
  • (C) Comparison: Placebo/sham treatments, conventional rehabilitation
  • (O) Outcome measure: NLUTD Assessment Tool scores, urodynamic parameters
We considered eligible randomized controlled clinical trials (RCTs), observational and quasi experimental studies; systematic review were only considered for citation searching, according to the PRISMA model.
Exclusion criteria regarded studies involving children; patients with non-neurogenic NLUTD; patients who underwent a rehabilitation program focused on PTNS (functional electrostimulation), sacral neuromodulation, and pelvic floor muscle training (PFMT); patients who were treated with botulinum toxin or surgery; or where the outcomes were pain-related questionnaires; all publications different from inclusion criteria.

2.2. Data Extraction

After removing duplicates, two reviewers independently extracted records through Zotero Software, and then proceeded to the screening for title and abstract in accordance with the inclusion criteria. In cases of disagreement, consensus was reached through discussion with a third reviewer. Includible articles were then selected for full text retrieval; after excluding not retrieved articles, full text reading guided the final inclusion in the last stage of the present review. Data from included studies were exported on a customized Microsoft Excel spreadsheet. The following data were extracted: first author, publication year, aims, design, intervention, sampling, outcome measures, summary of findings, and limitations. Data extraction was finally completed with methodological scores (Pedro and Cochrane tools).

2.3. Appraisal

The study quality was independently assessed by two reviewers using the PEDro scale [46]. According to the PEDro scale, the studies were classified as excellent (9–10 points), good (6–8 points), fair (4–5 points), or poor (<4 points). Additionally, the Cochrane Risk-of-Bias tool (RCTS/Observational studies versions as appropriate) was used for bias risk assessment [47]. Any disagreements were resolved by a third reviewer.

3. Results

As described in Figure 1, a total of 5993 results emerged from the overall database search (Supplementary Material S1), of which 426 were excluded after screening for duplicates. The remaining 5567 papers were screened for inclusion according to title/abstract reading, excluding book chapters, conference acts, case series/case reports, animal studies and preclinical models, essays, expert opinion papers, and articles in languages other than English. After this screening, 104 were included for full-text retrieval. Twenty-one studies were not retrieved through our librarian system; finally, 83 papers were assessed for eligibility. Of these, 64 involved combined interventions (including neuromodulation/botulinum toxin/PTNS) and 17 involved PFMT sessions. Finally, two articles were included. Citation searches led to the identification of one more article; therefore, three studies were included in this systematic review.
Two of the included studies were non-randomized double-cohort studies [48,49], while the remaining study was a randomized controlled trial [50]. Two studies [48,49] were conducted by the same author, who had previously carried out similar studies on animals. The data extracted from these studies are reported in Table 1.

3.1. Quality Assessment

In terms of methodological evaluation, the PEDro score revealed an overall medium quality of evidence: the scores of the first [48], second [49], and third [50] studies were 5/10, 6/10, and 7/10 points, respectively. The main reason why the included studies did not reach the highest levels of the PEDro scale was the impossibility of applying blinding strategies; given the nature of the interventions, in fact, patients and operators were aware of which treatment was being applied.
A low risk-of-bias emerged based on the Cochrane Risk-of-Bias tool (the observational studies tool for the cohort studies [48,49] and the RCTS tools for the study by Williams et al. [50]).

3.2. Synthesis of Results

In the three studies, 40 patients were involved (mean age: 29.5 years, range 19–62 years), of whom 35 were men and 5 were women. A summary of the included studies is presented in Table 1. All studies were conducted in the United States.
Hubscher et al.’s studies [48,49] involved 12 [48] and 22 [49] patients, respectively, with the development of overactive bladder/neurological bowel after SCI. The study by Williams et al. [50] involved six patients with a mean age of 28.5 years (range: 24–49 years), who were at least 6-months post-injury, with SCI at or above the T10 vertebral level. Patients met the requirements for the Ekso and Lokomat devices and had NLUTD.

3.3. Intervention

In the first study by Hubscher et al. [48], eight patients underwent 80 (1 h/day) physiotherapy treatments based on treadmill walk training, assisted by a bodyweight support system. Alternatively, locomotor and standing training (weight-bearing without stepping) were performed by the other four patients. Therapists utilized manual facilitation to guide gait training and maximize neuromuscular activity. Treadmill speed was set to a normal walking range (0.89–1.34 m/s) and was varied 25% of the time. In the weight-bearing system training, the participants were instructed to reach and maintain a standing position for 60 min. The remaining four participants in the study received only the usual care.
In the second study by Hubscher et al. [49], 12 participants were selected from the previous study’s standing-only group [48], while an additional 10 participants were selected for inclusion in the arm-training cohort. The first group underwent the same standing training as in the previous study (with a weight-bearing system or customized standing); the remaining group performed 1 h of upper-limb cycle ergometer training, in four to five sessions per week. As patients’ abilities (first endurance) improved, exercise was made more strenuous by increasing resistance.
In the RCT by Williams et al. [50], six participants were randomized to receive either a Lokomat- or Ekso-based walking program. The training intervention included 36–45-min walking sessions of exoskeleton training, three times a week for over 12 weeks.

3.4. Outcomes

Regarding bladder outcome measures, all three studies focused on urodynamic examination and specific urinary-referred questionnaires: Hubscher et al. [48,49] used the International Spinal Cord Injury Data Sets Questionnaires–Urodynamics and Lower Urinary Tract Function, whereas Williams et al. [50] used the Qualiveen-30 questionnaire and a bladder diary. Data were collected using a questionnaire administered before and after rehabilitation treatment.
In the two cohort studies [48,49], pre- and post-intervention urodynamics and cystometry were carried out by the same nurse, whereas in the RCT, it was carried out by a blinded assessor and analyzed by a urologist.
Hubscher et al. [48] reported significantly higher detrusorial contractions, lower pressure levels, and an increase in bladder capacity in the lower-limb training group. Furthermore, increases in bladder contraction capacity and detrusor contraction length were also observed. In the second study by this group [49], standing training alone had no significant urological benefits, whereas the upper-limb strengthening group showed significant changes in bladder pressure (lower values) and compliance (higher values), although no change was registered in bladder filling volume or voiding efficacy.
In the third study [50], slight and non-significant benefits in urodynamic examination parameters were observed, probably because of the small number of participants in the standing training treatment.

3.5. Lower Urinary Tract Questionnaire and Secondary Outcomes

In terms of secondary outcomes, Hubsher [48] considered the following dataset to investigate bowel, lower urinary tract symptoms, and sexual functions: The International SCI Data Sets Questionnaires for Urodynamics and Lower Urinary Tract Function, Bowel Function, Female Sexual, and Reproductive function/Male Sexual Function. In the second study [49], he further integrated the 15-item International Index of Erectile Function/the 19-item Female Sexual Function Index.
In the study of Williams [50], secondary outcome regarded pelvic floor muscles activation through electromyography, a three-days bladder diary, the SF-Qualiveen questionnaire, speed/walking distance, and effort perception during robotic gait training.
The only significant results for secondary outcome were reported by Hubsher [48,49]: lower urinary tract function dataset questionnaires revealed that nocturia episodes and incontinence were reduced by the end of the training, but the frequency of catheterization remained unchanged [48,49]. In addition, authors reported improvements in fecal incontinence, with fewer referred episodes, a significant decrease in defecation time, and an improvement in sexual desire following treatment; other questionnaires reported only minimal and not significant changes. Williams [50] reported improvements in training related outcomes (speed/distance) and a greater activation of pelvic floor muscles in the Ekso group, while no changes were detected in any of the NLUTD-related questionnaires.

4. Discussion

This systematic review investigated whether exercise applied to the lower limbs and changes in neurogenic dysfunction of the lower urinary tract were related. In the three studies included, urodynamics and specific bladder functionality questionnaires provided preliminary evidence of improvement in NLUTD following lower limb stimulation via weight-suspension walking training, and a greater PFM activation following an exoskeleton-based training. The evidence in this systematic review always refers to SCI population, as there was no experience dealing with other NLUTD forms.
To date, a complex model of NLUTD neuro-pathology is being introduced in research [1,51], with symptoms that vary depending on disease localization, evolution, and consequences (so the current NLUTD classification may only serve as a general framework [52]). Central control of micturition has been extensively studied in the past [53]. In the case of suprapontine lesions, two distinct clinical subtypes determining “urgency” are characterized by the presence or absence of detrusor overactivity (DO) [7]. This is particularly important in SCI individuals, where profound alterations of the detrusor afferents occur. As demonstrated in experimental animals, the activation of unmyelinated C-afferent fibers [54,55,56] alters the normal spinal afferents guaranteed by A-delta fibers [57].
Lower urinary tract disorders after SCI represent a severe physical impairment, with a marked psychological impact and adverse effects on quality of life and autonomy, and impose a barrier on social relationships [58,59,60,61]. Rehabilitative therapeutic strategies have always considered motor recovery as central [62], and only after the introduction of intermittent catheterization practice was it possible to observe a reduction in long-term damage to the upper urinary tract [63,64]. To date, the possible consequences of motor exercise on lower urinary tract, intestinal, and sexual dysfunction have not been well studied; in this scenario, locomotor training is classically considered to improve cardiovascular function, strength, and mobility [65,66,67,68,69]. Regarding its effects on NLUTD, several animal studies have demonstrated positive effects of locomotor training [70,71,72]; in humans, the efficacy of exercise on lower urinary tract dysfunction initially appeared as an anecdotal observation and then as a secondary outcome of research using exoskeletons [42], and of epidural stimulation in patients with complete injuries [73]. The hypothesis is based on evidence regarding the effects of PFMT on detrusor function [74,75,76] in individuals with non-neurological and neurological conditions [77,78]. Inhibitory action of PFMT can be induced by the synergistic activity of the lower limb muscles and the pelvic floor itself [75,79], and by connections between different cortical areas involved in pelvic floor activity and lower limb motor areas [39,80]. Based on studies of the overlap of cortical areas controlling the voluntary recruitment of the pelvic floor and some lower limb muscles [81], the effectiveness of locomotor training in incomplete SCI may be determined by the activation of spinal mechanisms induced by muscle afferents [82], in a manner entirely overlapping with the effect induced by stimulation of the tibial nerve [83]. In addition, activating nerve pathways that control coordination of locomotor function could induce adaptive changes in neural networks within the lumbosacral cord, likely including those controlling bladder [84]. Data by our review seems to confirm this hypothesis, with preliminary findings of effectiveness for leg-related exercise on NLUTD control [48,49,50]; despite this, an absolute need to deepen this argument emerged: we do not exactly know neither the optimal dosage of stimulation, nor what is the best form of training to achieve lasting results, nor long-term data (included studies were all pre-post).
In order to better explain the significance of our findings, we conducted a post hoc power analysis using G-Power software [85], using the available data from the Hubscher et al. study, which included 22 patients. The results indicated that the power of the study was low, suggesting that the study may not have been sufficiently powered to detect significant effects of the upper limb strengthening intervention. This limitation should be considered when interpreting the results and highlights the need for future studies with larger sample sizes and adequate power to more accurately assess the intervention’s efficacy. Nevertheless, the preliminary data may provide useful insights for further investigations, as already underlined by precedent literature [64,86].
The results of this review represent a first step toward planning future research and further exploring the role of specific lower-limb exercises in inhibiting an overactive bladder. Future studies should address the current heterogeneity in testing and evaluating the effect of lower limb motor exercises on NLUTD. Researchers should primarily test larger populations, overcoming the current gap in research focusing exclusively on spinal cord injury.
Furthermore, they should study single interventions rather than combinations of several techniques, in order to allow for a true evaluation of their effects. Finally, a higher degree of uniformity is needed in the definition of PROMS (patient-reported outcome measures), as the high variability of datasets hinders standardization and comparability between different studies.
There were some limitations of the present review. First of all, the low number of included papers and low sample sizes only allow us to infer preliminary evidence with respect to the use of lower limb training in the modulation of urinary neurogenic dysfunction. Moreover, studies had different designs and methodologies (two non-randomized cohort studies and one RCT), and this represents an additional difficulty of comparison. Finally, the interventions had the same rationale but were radically different (treadmill or standing weight-supported training, exoskeleton) even in terms of frequency and energy expenditure by the patient.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/bioengineering12020127/s1, S1: Search strategy among database.

Author Contributions

Conceptualization, G.L. and G.C.; methodology, G.C.; software, C.C.; validation, C.C.; formal analysis, G.C. and M.F.; investigation, M.F. and P.G.; resources, G.L. and D.G.; data curation, G.L., G.C. and C.C.; writing—original draft preparation, G.C., M.F. and G.L.; writing—review and editing, G.C., M.F., G.L., D.G., P.G. and C.C.; visualization, G.L.; supervision, G.L.; project administration, G.L. and D.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are available within the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Panicker, J.N.; Fowler, C.J.; Kessler, T.M. Lower urinary tract dysfunction in the neurological patient: Clinical assessment and management. Lancet Neurol. 2015, 14, 720–732. [Google Scholar] [CrossRef] [PubMed]
  2. Panicker, J.N. Neurogenic bladder: Epidemiology, diagnosis, and management. Semin. Neurol. 2020, 40, 569–579. [Google Scholar] [CrossRef] [PubMed]
  3. Drake, M.J. Management and rehabilitation of neurologic patients with lower urinary tract dysfunction. Handb. Clin. Neurol. 2015, 130, 451–468. [Google Scholar] [CrossRef]
  4. Schurch, B.; Tawadros, C.; Carda, S. Dysfunction of lower urinary tract in patients with spinal cord injury. Handb. Clin. Neurol. 2015, 130, 247–267. [Google Scholar] [CrossRef]
  5. Qin, C.; Wang, Y.; Gao, Y. Overactive bladder symptoms within the nervous system: A focus on etiology. Front. Physiol. 2021, 12, 747144. [Google Scholar] [CrossRef]
  6. Averbeck, M.A.; Madersbacher, H. Follow-up of the neuro-urological patient: A systematic review. BJU Int. 2015, 115 (Suppl. S6), 39–46. [Google Scholar] [CrossRef]
  7. Peyronnet, B.; Mironska, E.; Chapple, C.; Cardozo, L.; Oelke, M.; Dmochowski, R.; Amarenco, G.; Gamé, X.; Kirby, R.; Van Der Aa, F.; et al. A comprehensive review of overactive bladder pathophysiology: On the way to tailored treatment. Eur. Urol. 2019, 75, 988–1000. [Google Scholar] [CrossRef]
  8. Wyndaele, J.; Madersbacher, H.; Castro, D.; Chartier-Kasler, E.; Igawa, Y.; Kovindha, H. Chapter 17: Neurologic urinary and fecal incontinence. In Incontinence; Abrams, P., Cardozo, L., Khoury, S., Wein, A., Eds.; Health Publications: Plymouth, UK, 2004; Volume 2. [Google Scholar]
  9. Wyndaele, J.; Kovindha, H.; Madersbacher, H.; Castro, D.; Chartier-Kasler, E.; Igawa, Y. Chapter 10: Neurogenic bladder and bowel. In Incontinence. In Incontinence; Abrams, P., Cardozo, L., Khoury, S., Wein, A., Eds.; Health Publications: Plymouth, UK, 2009; Volume 1. [Google Scholar]
  10. Sakakibara, R. Lower urinary tract dysfunction in patients with brain lesions. Handb. Clin. Neurol. 2015, 130, 269–287. [Google Scholar] [CrossRef]
  11. Weld, K.J.; Dmochowski, R.R. Association of level of injury and bladder behavior in patients with post-traumatic spinal cord injury. Urology 2000, 55, 490–494. [Google Scholar] [CrossRef]
  12. Podnar, S.; Vodušek, D.B. Lower urinary tract dysfunction in patients with peripheral nervous system lesions. Handb. Clin. Neurol. 2015, 130, 203–224. [Google Scholar] [CrossRef]
  13. Brocklehurst, J.C.; Andrews, K.; Richards, B.; Laycock, P.J. Incidence and correlates of incontinence in stroke patients. J. Am. Geriatr. Soc. 1985, 33, 540–542. [Google Scholar] [CrossRef] [PubMed]
  14. Blok, B.; Castro-Diaz, D.; Del Popolo, G.; Groen, J.; Hamid, R.; Karsenty, G.; Kessler, T.M.; Pannek, J.; Ecclestone, H.; Musco, S.; et al. EEAU Guidelines on Neurourology; European Association of Urology: Arnhem, The Netherlands, 2023. [Google Scholar]
  15. Finazzi Agrò, E.; Salvatore, S.; Braga, A.; DeLancey, J.; Fernando, R.; Iacovelli, V. Committee 3: Pathophysiology of urinary incontinence, pelvic organ prolapse, and faecal incontinence. In International Consultation on Incontinence, 7th ed.; Cardozo, L., Rovner, E., Wagg, A., Wein, A., Abrams, P., Eds.; Health Publications Ltd.: Plymouth, UK, 2023. [Google Scholar]
  16. Konstantinidis, C.; Kratiras, Z.; Samarinas, M.; Skriapas, K. Optimal bladder diary duration for patients with supraspinal neurogenic lower urinary tract dysfunction. Int. Braz. J. Urol. 2016, 42, 766–772. [Google Scholar] [CrossRef]
  17. Best, K.L.; Ethans, K.; Craven, B.C.; Noreau, L.; Hitzig, S.L. Identifying and classifying quality of life tools for neurogenic bladder function after spinal cord injury: A systematic review. J. Spinal Cord. Med. 2017, 40, 505–529. [Google Scholar] [CrossRef] [PubMed]
  18. Bonniaud, V.; Bryant, D.; Parratte, B.; Guyatt, G. Development and validation of the short form of a urinary quality of life questionnaire: SF-Qualiveen. J. Urol. 2008, 180, 2592–2598. [Google Scholar] [CrossRef]
  19. Bellucci, C.H.; Wöllner, J.; Gregorini, F.; Birnböck, D.; Kozomara, M.; Mehnert, U.; Kessler, T.M. Neurogenic lower urinary tract dysfunction: Do we need same-session repeat urodynamic investigations? J. Urol. 2012, 187, 1318–1323. [Google Scholar] [CrossRef]
  20. Schöps, T.F.; Schneider, M.P.; Steffen, F.; Ineichen, B.V.; Mehnert, U.; Kessler, T.M. Neurogenic lower urinary tract dysfunction (NLUTD) in patients with spinal cord injury: Long-term urodynamic findings. BJU Int. 2015, 115 (Suppl. S6), 33–38. [Google Scholar] [CrossRef]
  21. Rosier, P.F.W.M.; Schaefer, W.; Lose, G.; Goldman, H.B.; Guralnick, M.; Eustice, S.; Dickinson, T.; Hashim, H. International Continence Society Good Urodynamic Practices and Terms 2016: Urodynamics, uroflowmetry, cystometry, and pressure-flow study. Neurourol. Urodyn. 2017, 36, 1243–1260. [Google Scholar] [CrossRef]
  22. Drake, M.J.; Doumouchtsis, S.K.; Hashim, H.; Gammie, A. Fundamentals of urodynamic practice, based on International Continence Society good urodynamic practices recommendations. Neurourol. Urodyn. 2018, 37, S50–S60. [Google Scholar] [CrossRef] [PubMed]
  23. Lucas, E. Medical management of neurogenic bladder for children and adults: A review. Top. Spinal Cord. Inj. Rehabil. 2019, 25, 195–204. [Google Scholar] [CrossRef]
  24. Madhuvrata, P.; Singh, M.; Hasafa, Z.; Abdel-Fattah, M. Anticholinergic drugs for adult neurogenic detrusor overactivity: A systematic review and meta-analysis. Eur. Urol. 2012, 62, 816–830. [Google Scholar] [CrossRef]
  25. Zhang, D.; Sun, F.; Yao, H.; Bao, X.; Wang, D.; Cui, Y.; Wu, J. The efficacy and safety of Mirabegron for the treatment of neurogenic lower urinary tract dysfunction: A systematic review and meta-analysis. Front. Pharmacol. 2021, 12, 756582. [Google Scholar] [CrossRef]
  26. Hu, J.C.; Hsu, L.N.; Lee, W.C.; Chuang, Y.C.; Wang, H.J. Role of urological botulinum toxin-A injection for overactive bladder and voiding dysfunction in patients with Parkinson’s disease or post-stroke. Toxins 2023, 15, 166. [Google Scholar] [CrossRef]
  27. Ni, J.; Wang, X.; Cao, N.; Si, J.; Gu, B. Is repeat botulinum toxin A injection valuable for neurogenic detrusor overactivity? A systematic review and meta-analysis. Neurourol. Urodyn. 2018, 37, 542–553. [Google Scholar] [CrossRef]
  28. Huang, J.; Fan, Y.; Zhao, K.; Yang, C.; Zhao, Z.; Chen, Y.; Yang, J.; Wang, T.; Qu, Y. Comparative efficacy of neuromodulation technologies for overactive bladder in adults: A network meta-analysis of randomized controlled trials. Neuromodulation 2023, 26, 1535–1548. [Google Scholar] [CrossRef]
  29. Tahmasbi, F.; Salehi-Pourmehr, H.; Naseri, A.; Ghaderi, S.; Javadi-Farid, F.; Hajebrahimi, S.; Sedigh, O.; Soleimanzadeh, F. Effects of posterior tibial nerve stimulation (PTNS) on lower urinary tract dysfunction: An umbrella review. Neurourol. Urodyn. 2024, 43, 494–515. [Google Scholar] [CrossRef]
  30. Averbeck, M.A.; Moreno-Palacios, J.; Aparicio, A. Is there a role for sacral neuromodulation in patients with neurogenic lower urinary tract dysfunction? Int. Braz. J. Urol. 2020, 46, 891–901. [Google Scholar] [CrossRef]
  31. De Wachter, S.; Knowles, C.H.; Elterman, D.S.; Kennelly, M.J.; Lehur, P.A.; Matzel, K.E.; Engelberg, S.; Van Kerrebroeck, P.E.V. New technologies and applications in sacral neuromodulation: An update. Adv. Ther. 2020, 37, 637–643. [Google Scholar] [CrossRef]
  32. Evancho, A.; Tyler, W.J.; McGregor, K. A review of combined neuromodulation and physical therapy interventions for enhanced neurorehabilitation. Front. Human Neurosci. 2023, 17, 1151218. [Google Scholar] [CrossRef]
  33. Lúcio, A.C.; Campos, R.M.; Perissinotto, M.C.; Miyaoka, R.; Damasceno, B.P.; D’ancona, C.A. Pelvic floor muscle training in the treatment of lower urinary tract dysfunction in women with multiple sclerosis. Neurourol. Urodyn. 2010, 29, 1410–1413. [Google Scholar] [CrossRef]
  34. Lúcio, A.C.; Perissinotto, M.C.; Natalin, R.A.; Prudente, A.; Damasceno, B.P.; D’ancona, C.A. A comparative study of pelvic floor muscle training in women with multiple sclerosis: Its impact on lower urinary tract symptoms and quality of life. Clin. 2011, 66, 1563–1568. [Google Scholar] [CrossRef]
  35. Shin, D.C.; Shin, S.H.; Lee, M.M.; Lee, K.J.; Song, C.H. Pelvic floor muscle training for urinary incontinence in female stroke patients: A randomized, controlled and blinded trial. Clin. Rehabil. 2016, 30, 259–267. [Google Scholar] [CrossRef]
  36. Tibaek, S.; Jensen, R.; Lindskov, G.; Jensen, M. Can quality of life be improved by pelvic floor muscle training in women with urinary incontinence after ischemic stroke? A randomized, controlled and blinded study. Int. Urogynecol. J. 2004, 15, 117–123. [Google Scholar] [CrossRef]
  37. Tibaek, S.; Gard, G.; Jensen, R. Is there a long-lasting effect of pelvic floor muscle training in women with urinary incontinence after ischemic stroke? A 6-month follow-up study. Int. Urogynecol. J. 2007, 18, 281–287. [Google Scholar] [CrossRef]
  38. Tibaek, S.; Gard, G.; Jensen, R. Pelvic floor muscle training is effective in women with urinary incontinence after stroke: A randomized, controlled and blinded study. Neurourol. Urodyn. 2005, 24, 348–357. [Google Scholar] [CrossRef]
  39. Asavasopon, S.; Rana, M.; Kirages, D.J.; Yani, M.S.; Fisher, B.E.; Hwang, D.H.; Lohman, E.B.; Berk, L.S.; Kutch, J.J. Cortical activation associated with muscle synergies of the human male pelvic floor. J. Neurosci. 2014, 34, 13811–13818. [Google Scholar] [CrossRef]
  40. Santana, N.N.M.; Silva, E.H.A.; Santos, S.F.D.; Bezerra, L.L.F.; da Silva, M.M.O.; Cavalcante, J.S.; Fiuza, F.P.; Morais, d.G.P.L.A.; Engelberth, R.C. Neuronal Stability, Volumetric Changes, and Decrease in GFAP Expression of Marmoset (Callithrix jacchus) Subcortical Visual Nuclei During Aging. J. Comp. Neurol. 2024, 532, e25649. [Google Scholar] [CrossRef]
  41. Baunsgaard, C.B.; Nissen, U.V.; Brust, A.K.; Frotzler, A.; Ribeill, C.; Kalke, Y.B.; León, N.; Gómez, B.; Samuelsson, K.; Antepohl, W.; et al. Exoskeleton gait training after spinal cord injury: An exploratory study on secondary health conditions. J. Rehabil. Med. 2018, 50, 806–813. [Google Scholar] [CrossRef]
  42. Schalow, G.; Jaigma, P.; Belle, V.K. Near-total functional recovery achieved in partial cervical spinal cord injury (50% injury) after 3 years of coordination dynamics therapy. Electromyogr. Clin. Neurophysiol. 2009, 49, 67–91. [Google Scholar]
  43. Schalow, G. Scientific basis for learning transfer from movements to urinary bladder functions for bladder repair in human patients with CNS injury. Electromyogr. Clin. Neurophysiol. 2010, 50, 339–395. [Google Scholar]
  44. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Int. J. Surg. 2010, 8, 336–341. [Google Scholar] [CrossRef]
  45. Lamberti, G. Can a lower limb-centered movement training inhibit overactive bladder? Systematic review of literature. Inplasy Protoc. 2022, 22, 202270099. [Google Scholar] [CrossRef]
  46. de Morton, N.A. The PEDro scale is a valid measure of the methodological quality of clinical trials: A demographic study. Aust. J. Physiother. 2009, 55, 129–133. [Google Scholar] [CrossRef] [PubMed]
  47. Higgins, J.P.; Altman, D.G.; Gøtzsche, P.C.; Jüni, P.; Moher, D.; Oxman, A.D.; Savovic, J.; Schulz, K.F.; Weeks, L.; Sterne, J.A. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011, 343, d5928. [Google Scholar] [CrossRef]
  48. Hubscher, C.H.; Herrity, A.N.; Williams, C.S.; Montgomery, L.R.; Willhite, A.M.; Angeli, C.A.; Harkema, S.J. Improvements in bladder, bowel and sexual outcomes following task-specific locomotor training in human spinal cord injury. PLoS ONE 2018, 13, e0190998. [Google Scholar] [CrossRef]
  49. Hubscher, C.H.; Wyles, J.; Gallahar, A.; Johnson, K.; Willhite, A.; Harkema, S.; Herrity, A.N. Impact of different forms of activity-based recovery training on bladder, bowel and sexual function following spinal cord injury. Arch. Phys. Med. Rehabil. 2021, 102, 865–873. [Google Scholar] [CrossRef]
  50. Williams, A.M.M.; Deegan, E.; Walter, M.; Stothers, L.; Lam, T. Exoskeleton gait training to improve lower urinary tract function in people with motor-complete spinal cord injury: A randomized pilot trial. J. Rehabil. Med. 2021, 53, jrm00222. [Google Scholar] [CrossRef]
  51. Gajewski, J.B.; Drake, M.J. Neurological lower urinary tract dysfunction essential terminology. Neurourol. Urodyn. 2018, 37, S25–S31. [Google Scholar] [CrossRef]
  52. Holstege, G.; Griffiths, D.; de Wall, H.; Dalm, E. Anatomical and physiological observations on supraspinal control of bladder and urethral sphincter muscles in the cat. J. Comp. Neurol. 1986, 250, 449–461. [Google Scholar] [CrossRef]
  53. Griffiths, D.; Tadic, S.D. Bladder control, urgency, and urge incontinence: Evidence from functional brain imaging. Neurourol. Urodyn. 2008, 27, 466–474. [Google Scholar] [CrossRef]
  54. Tadic, S.D.; Griffiths, D.; Schaefer, W.; Murrin, A.; Clarkson, B.; Resnick, N.M. Brain activity underlying impaired continence control in older women with overactive bladder. Neurourol. Urodyn. 2012, 31, 652–658. [Google Scholar] [CrossRef]
  55. Häbler, H.J.; Jänig, W.; Koltzenburg, M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J. Physiol. 1990, 425, 545–562. [Google Scholar] [CrossRef] [PubMed]
  56. Yoshimura, N. Bladder afferent pathway and spinal cord injury: Possible mechanisms inducing hyperreflexia of the urinary bladder. Prog. Neurobiol. 1999, 57, 583–606. [Google Scholar] [CrossRef] [PubMed]
  57. Horst, M.; Heutschi, J.; van den Brand, R.; Andersson, K.E.; Gobet, R.; Sulser, T.; Courtine, G.; Eberli, D. Multisystem neuroprosthetic training improves bladder function after severe spinal cord injury. J. Urol. 2013, 189, 747–753. [Google Scholar] [CrossRef] [PubMed]
  58. Gajeski, J.B.; Madersbacher, H. Classification and terminology of neurogenic LUT dysfunction. In Handbook of Neurourology, 1st ed.; Liao, L., Madersbacher, H., Eds.; Springer Nature: Singapore, 2023. [Google Scholar]
  59. Hamid, R.; Averbeck, M.A.; Chiang, H.; Garcia, A.; Al Mousa, R.T.; Oh, S.J.; Patel, A.; Plata, M.; Del Popolo, G. Epidemiology and pathophysiology of neurogenic bladder after spinal cord injury. World J. Urol. 2018, 36, 1517–1527. [Google Scholar] [CrossRef]
  60. Craig, A.; Nicholson Perry, K.; Guest, R.; Tran, Y.; Middleton, J. Adjustment following chronic spinal cord injury: Determining factors that contribute to social participation. Br. J. Health Psychol. 2015, 20, 807–823. [Google Scholar] [CrossRef]
  61. Piatt, J.A.; Nagata, S.; Zahl, M.; Li, J.; Rosenbluth, J.P. Problematic secondary health conditions among adults with spinal cord injury and its impact on social participation and daily life. J. Spinal Cord. Med. 2016, 39, 693–698. [Google Scholar] [CrossRef]
  62. Tate, D.G.; Wheeler, T.; Lane, G.I.; Forchheimer, M.; Anderson, K.D.; Biering-Sorensen, F.; Cameron, A.P.; Santacruz, B.G.; Jakeman, L.B.; Kennelly, M.J.; et al. Recommendations for evaluation of neurogenic bladder and bowel dysfunction after spinal cord injury and/or disease. J. Spinal Cord. Med. 2020, 43, 141–164. [Google Scholar] [CrossRef]
  63. Mashola, M.K.; Korkie, E.; Mothabeng, D.J. Exploring the experience of living with pain after spinal cord injury: A qualitative study. Behav. Neurol. 2024, 2024, 9081530. [Google Scholar] [CrossRef]
  64. Hubscher, C.H.; Montgomery, L.R.; Fell, J.D.; Armstrong, J.E.; Poudyal, P.; Herrity, A.N.; Harkema, S.J. Effects of exercise training on urinary tract function after spinal cord injury. Am. J. Physiol. Ren. Physiol. 2016, 310, 1258–1268. [Google Scholar] [CrossRef]
  65. Timoney, A.G.; Shaw, P.J. Urological outcome in female patients with spinal cord injury: The effectiveness of intermittent catheterisation. Paraplegia 1990, 28, 556–563. [Google Scholar] [CrossRef]
  66. Perrouin-Verbe, B.; Labat, J.J.; Richard, I.; Mauduyt de la Greve, I.; Buzelin, J.M.; Mathe, J.F. Clean intermittent catheterisation from the acute period in spinal cord injury patients. Long term evaluation of urethral and genital tolerance. Paraplegia 1995, 33, 619–624. [Google Scholar] [CrossRef] [PubMed]
  67. Behrman, A.L.; Lawless-Dixon, A.R.; Davis, S.B.; Bowden, M.G.; Nair, P.; Phadke, C.; Hannold, E.M.; Plummer, P.; Harkema, S.J. Locomotor training progression and outcomes after incomplete spinal cord injury. Phys. Ther. 2005, 85, 1356–1371. [Google Scholar] [CrossRef] [PubMed]
  68. Dietz, V.; Harkema, S.J. Locomotor activity in spinal cord-injured persons. J. Appl. Physiol. 2004, 96, 1954–1960. [Google Scholar] [CrossRef] [PubMed]
  69. Harkema, S.J.; Hillyer, J.; Schmidt-Read, M.; Ardolino, E.; Sisto, S.A.; Behrman, A.L. Locomotor training as a treatment of spinal cord injury and in the progression of neurologic rehabilitation. Arch. Phys. Med. Rehabil. 2012, 93, 1588–1597. [Google Scholar] [CrossRef]
  70. Pedersen, E.; Petersen, T.; Schrøder, H.D. Relation between flexor spasms, uninhibited detrusor contractions and anal sphincter activity. J. Neurol. Neurosurg. Psychiatry 1986, 49, 273–277. [Google Scholar] [CrossRef]
  71. Ward, P.J.; Herrity, A.N.; Smith, R.R.; Willhite, A.; Harrison, B.J.; Petruska, J.C.; Harkema, S.J.; Hubscher, C.H. Novel multi-system functional gains via task-specific training in spinal cord injured male rats. J. Neurotrauma 2014, 31, 819–833. [Google Scholar] [CrossRef]
  72. Ward, P.J.; Herrity, A.N.; Harkema, S.J.; Hubscher, C.H. Training-induced functional gains following SCI. Neural Plast. 2016, 2016, 4307694. [Google Scholar] [CrossRef]
  73. Shafik, A.; Shafik, I.A. Overactive bladder inhibition in response to pelvic floor muscle exercises. World J. Urol. 2003, 20, 374–377. [Google Scholar] [CrossRef]
  74. Burgio, K.L. Update on behavioral and physical therapies for incontinence and overactive bladder: The role of pelvic floor muscle training. Curr. Urol. Rep. 2013, 14, 457–464. [Google Scholar] [CrossRef]
  75. Amorim, A.C.; Cacciari, L.P.; Passaro, A.C.; Silveira, S.R.B.; Amorim, C.F.; Loss, J.F.; Sacco, I.C.N. Effect of combined actions of hip adduction/abduction on the force generation and maintenance of pelvic floor muscles in healthy women. PLoS ONE 2017, 12, e0177575. [Google Scholar] [CrossRef]
  76. Cardozo, L.; Stanton, S.L.; Hafner, J.; Allan, V. Biofeedback in the treatment of detrusor instability. Br. J. Urol. 1978, 50, 250–254. [Google Scholar] [CrossRef] [PubMed]
  77. Elmelund, M.; Biering-Sorensen, F.; Due, U.; Klarskov, N. The effect of pelvic floor muscle training and intravaginal electrical stimulation on urinary incontinence in women with incomplete spinal cord injury: An investigator-blinded parallel randomized clinical trial. Int. Urogynecol. J. 2018, 29, 1597–1606. [Google Scholar] [CrossRef] [PubMed]
  78. Gaikwad, A.J.; Kanase, S.B. Effect of structured bladder training in urinary incontinence. Indian J. Physiother. Occup. Ther. 2020, 14, 30–36. [Google Scholar]
  79. Kocjancic, E.; Chung, E.; Garzon, J.A.; Haylen, B.; Iacovelli, V.; Jaunarena, J.; Locke, J.; Millman, A.; Nahon, I.; Ohlander, S.; et al. International Continence Society (ICS) report on the terminology for sexual health in men with lower urinary tract (LUT) and pelvic floor (PF) dysfunction. Neurourol. Urodyn. 2022, 41, 140–165. [Google Scholar] [CrossRef]
  80. Schrum, A.; Wolff, S.; van der Horst, C.; Kuhtz-Buschbeck, J.P. Motor cortical representation of the pelvic floor muscles. J. Urol. 2011, 186, 185–190. [Google Scholar] [CrossRef]
  81. Fowler, S.B. Pelvic floor muscle training versus no treatment, or inactive control treatments, for urinary incontinence in women. Clin. Nurse Spec. 2011, 25, 226–227. [Google Scholar] [CrossRef]
  82. Martin, V.; Dousset, E.; Laurin, J.; Gondin, J.; Gautier, M.; Decherchi, P. Group III and IV muscle afferent discharge patterns after repeated lengthening and shortening actions. Muscle Nerve 2009, 40, 827–837. [Google Scholar] [CrossRef]
  83. Chen, G.; Larson, J.A.; Ogagan, P.D.; Shen, B.; Wang, J.; Roppolo, J.R.; de Groat, W.C.; Tai, C. Post-stimulation inhibitory effect on reflex bladder activity induced by activation of somatic afferent nerves in the foot. J. Urol. 2012, 187, 338–343. [Google Scholar] [CrossRef]
  84. Behrman, A.L.; Harkema, S.J. Locomotor training after human spinal cord injury: A series of case studies. Phys. Ther. 2000, 80, 688–700. [Google Scholar] [CrossRef]
  85. Erdfelder, E.; Faul, F.; Buchner, A. GPOWER: A general power analysis program. Behav. Res. Methods Instrum. Comput. 1996, 28, 1–11. [Google Scholar] [CrossRef]
  86. Tai, C.; Shen, B.; Chen, M.; Wang, J.; Liu, H.; Roppolo, J.R.; de Groat, W.C. Suppression of bladder overactivity by activation of somatic afferent nerves in the foot. BJU Int. 2011, 107, 303–309. [Google Scholar] [CrossRef] [PubMed]
Bioengineering 12 00127 g001
Figure 1. Prisma flow diagram with indication of step-by-step screening of research records.
Figure 1. Prisma flow diagram with indication of step-by-step screening of research records.
Bioengineering 12 00127 g001
Table 1. Summary of included studies’ findings. Abbreviations: NLUTD: neurogenic lower urinary tract dysfunction; Exp: experimental; Con: control; N = number; LT: locomotor training; UDS: urodynamic study; SCI: spinal cord injury; EMG: electromyography; RPE: rating of perceived exertion; PFM: pelvic floor muscles; SF: short form; RCTs: randomized-controlled trials.
Table 1. Summary of included studies’ findings. Abbreviations: NLUTD: neurogenic lower urinary tract dysfunction; Exp: experimental; Con: control; N = number; LT: locomotor training; UDS: urodynamic study; SCI: spinal cord injury; EMG: electromyography; RPE: rating of perceived exertion; PFM: pelvic floor muscles; SF: short form; RCTs: randomized-controlled trials.
Author, DateCountryAim[s]DesignInterventionSamplingOutcome MeasuresSummary of FindingsStudy LimitationsMethodological Quality
Hubscher et al., 2018 [48]USAIdentify whether LT as can improve bladder, bowel, and sexual function in chronic SCI (more than two years post-injury) compared to usual caresProspective cohort study 12 participants with SCI.
Exp (8): 80 session of LT on a weight supported treadmill/LT plus 1 h/day stand training;
Cont (4): usual cares prosecution		Convenience sample UDS; The International SCI Data Sets Questionnaires for Urodynamics and Lower Urinary Tract Function, Bowel Function, Female Sexual, and Reproductive
function Male Sexual Function 		Significant increase in bladder capacity, voiding efficiency, detrusor contraction time, and decrease in voiding pressure post-training relative to baseline were found in Exp group. Questionnaires revealed a decrease in the frequency of nocturia and urinary incontinence, decrease in time for defecation, increase in sexual desire in Exp group. Small sample size Pedro score 5/10
Cochrane rob tool for cohort studies detected a low risk of bias
Hubscher et al., 2021 [49]USADetermine if urogenital and bowel improvements in chronic SCI could derive by weight-bearing training or from general exerciseProspective cohort study 22 individuals with chronic SCI, who were either enrolled in a prior stand training study (N = 12) or upper extremity training (N = 10)
Exp: 80 session of standing with weight support
Cont: 80 sessions of arm crank		Convenience sampleUDS; International SCI Data Set for lower urinary tract function; International SCI Data Set for bowel function; 15-item International Index of Erectile Function/the 19-item Female Sexual Function Index. All questionnaires were administered pre-/post-trainingUDS revealed no significant benefits for Exp group; in Cont group a reduction in bladder pressure and increase of compliance were reported. No differences were identified regarding bowel and sexual functionsSmall sample size Pedro score 6/10
Cochrane rob tool for cohort studies detected a low risk of bias
Williams et al., 2021 [50]CanadaTesting an exoskeleton-assisted intervention targeting NLUTD in people with motor-complete SCI; compare two exoskeleton programmes Randomized pilot trial 6 participants
Exp (4): 36 sessions of Ekso training
Cont (2): 36 sessions of Lokomat training		Convenience sampleMean speed, distance, and session RPE were taken for each participant during the first and last 5 sessions; EMG for PFM; UDS; 3-day bladder diary; SF-Qualiveen-30.All participants improved walking speed, distance but not RPE; PFM activity was greater in the Ekso group. UDS, bladder diary, and questionnaires did not clearly change in either group.Small sample sizePedro score 7/10
Cochrane rob tool for RCTs detected a low risk of bias
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Ciardi, G.; Giraudo, D.; Fontana, M.; Citterio, C.; Gandolfi, P.; Lamberti, G. Relevance of Leg Rehabilitation to Modulating Neurogenic Lower Urinary Tract Symptoms: A Systematic Review. Bioengineering 2025, 12, 127. https://doi.org/10.3390/bioengineering12020127

AMA Style

Ciardi G, Giraudo D, Fontana M, Citterio C, Gandolfi P, Lamberti G. Relevance of Leg Rehabilitation to Modulating Neurogenic Lower Urinary Tract Symptoms: A Systematic Review. Bioengineering. 2025; 12(2):127. https://doi.org/10.3390/bioengineering12020127

Chicago/Turabian Style

Ciardi, Gianluca, Donatella Giraudo, Milena Fontana, Chiara Citterio, Paola Gandolfi, and Gianfranco Lamberti. 2025. "Relevance of Leg Rehabilitation to Modulating Neurogenic Lower Urinary Tract Symptoms: A Systematic Review" Bioengineering 12, no. 2: 127. https://doi.org/10.3390/bioengineering12020127

APA Style

Ciardi, G., Giraudo, D., Fontana, M., Citterio, C., Gandolfi, P., & Lamberti, G. (2025). Relevance of Leg Rehabilitation to Modulating Neurogenic Lower Urinary Tract Symptoms: A Systematic Review. Bioengineering, 12(2), 127. https://doi.org/10.3390/bioengineering12020127

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