Background: Positive effect on pelvic floor muscle training (PFMT) has been reported in poststroke patients with neurogenic lower urinary tract dysfunction (NLUTD). The effects were measured by bladder diary, pelvic floor muscle function, lower urinary tract symptoms, sexuality, and quality of life. However, measurement on brain activity seems to be missing.
Objective: To identify studies which report brain activity measured by functional magnetic resonance imaging (fMRI) as a response to voluntary pelvic floor muscles (PFMs) contractions and PFMT.
Methods: A literature search in which six databases was screened for this review.
Results: Fourteen studies were identified all published during 2005 - 2020. Twelve studies reported data of brain activity as a response to voluntary PFMs contractions and two as a response to PFMT. The participants (n=277) were respectively healthy adults (n=172, 62%), males with prostate cancer (n=22, 8%), females with stress urinary incontinence (n=10, 4%), older women with urge urinary incontinence (n=62, 22%), and Multiple sclerosis (MS) patients with detrusor sphincter dyssynergia (n=11, 4%). No studies in stroke patients were identified.
All identified studies focused primarily on the cerebral control of micturition circuit, whereas the brain activity as response to voluntary PFMs contractions only played a role in the investigations.
Conclusions: The identified studies indicate that fMRI even provide valuable outcome data supporting clinical outcome data and provide knowledge of the underlying mechanisms in the brain and its control of the bladder by PFMs contractions and PFMT. However, no studies in stroke patients were identified.
There is a call for studies using fMRI, providing knowledge of the brain activity as a response to voluntary PFMs contractions and PFMT in stroke patients with NLUTD.
Brain activity, fMRI, Neurogenic lower urinary tract dysfunction, Outcome, Pelvic floor muscle training, Stroke
BOLD: Blood Oxygenation Level Dependent; fMRI Functional Magnetic Resonance Imaging; LUTS: Lower Urinary Tract Symptoms; M1: Primary motor cortex; MRI: Magnetic Resonance Imaging; NLUTD: Neurogenic Lower Urinary Tract Dysfunction; PAG: Periaqueductal Gray; PFMs: Pelvic Floor Muscles; PFMT: Pelvic Floor Muscle Training; PMC: Pontine Micturition Centre; SMA: Supplementary Motor Area; SUI: Stress Urinary Incontinence; UUI: Urge Urinary Incontinence
Pelvic floor muscle training (PFMT) has, over the past two decades, been recommended as first-line treatment for neurologically healthy patients with lower urinary tract symptoms (LUTS) [11-15]. Later on, a positive effect on PFMT in both male and female stroke patients with NLUTD have been reported [16-20]. The data indicating effect were measured on bladder-related outcomes such as bladder diary [16,18], pelvic floor muscles (PFMs) function [16,18], LUTS [16,18,19], sexuality  and QoL [19,22]. But measurement on brain activity seems to be lacking.
The central nervous system (CNS) controls the micturition cycle of storage and the voiding of urine. Micturition frequency in healthy adults with bladder capacity of 500 ml is typically about once every three to four hours, depending on fluid intake. Since the voiding takes two to three minutes, for 98-99% of the time, the bladder is in storage mode. In the healthy and continent state, when to void is determined by the perceived state of bladder fullness together with an assessment of the social appropriateness to do so. Bladder function is controlled by neural programs, which perform and locate to the pontine micturition centre (PMC) and are influenced by supra-pontine processes. The connections between the pons and the sacral spinal cord must be intact along with the peripheral innervation which arises from the pelvic and the pudendal nerves to innervate the bladder and the internal and external sphincter muscles to affect both storage and voiding.
The pelvic floor muscles (PFMs) is an important part of the adequate urethral closure function maintaining urinary continence. The PFMS is located deep within the pelvis and forms the bottom/base of the abdominal cavity. The median PFMs thickness at rest has been reported to be 9.3 mm (range 8.6 - 9.9 mm) increasing to 11.4 mm (range 10.8 - 12.5 mm) during contraction in healthy female . The PFMs include posteriorly located by coccygeus and the elevator ani (M. puborectalis, M. pubococcygeus and M. iliococcygeus) [24-26]. The PFMs are comprised of both passive and active components. The passive support function is mainly contributed by connective tissues (ligaments, fascia). In contrast, the active support function is mainly due to the pelvic floor muscles, which can be contracted voluntarily to elevate the pelvic floor thereby counterbalancing increased abdominal pressure and maintain the normal position of pelvic organs . The striated muscles include 70% of cases are the slow-twitch fibers (type I, aerobic oxidative) [28,29] and 30% of cases are fast-twitch fibers (type II, anaerobic-glycolytic) [30,31]. The PFMs can contract voluntarily and involuntarily contract and relax. The PFMs are directly innervated by S2-S4 efferents with the anterior urogenital diaphragm innervated by the pudendal nerve which arises from these sacral roots. Thus, the innervation needed for physiological bladder control is extensive, requiring supra-pontine inputs. Intact spinal connections between the pons and the sacral spinal cord must be intact, as well as the peripheral nerves .
PFMT aims to improve PFMs function. The training has to be in a systematic, intensive treatment program controlled by a specialized physiotherapist. The PFMT program consists of muscle awareness training, training of muscle strength, endurance and coordination. Details of the PFMT program has been published previously [16,18,33].
In nonhuman primates, studies have provided strong evidence of reorganisation following brain damage as a response to motor training [34,35] although, with variability . In stroke patients, these variabilities are associated with the extent and location of the brain damage.
According to Rossini et al., the injured human brain poststroke goes through a process of reorganisation and adaptive brain changes appear to go in line with motor training and rehabilitation, leading to improved functional outcomes . Early motor learning seems essential for a successful recovery, and motor learning mechanisms may be operative during spontaneous stroke recovery and interact with rehabilitative training [38,39].
Basic changes in the brain plasticity must be explored to improve functional rehabilitation in stroke patients.
Askim et al. reported in a longitudinal study, that motor network changes are associated with successful motor skill relearning after ischemic stroke  and Favre et al. reported in a meta-analysis that upper limb recovery after stroke is associated with the ipsilesional primary motor cortical activity .
Magnetic resonance imaging (MRI) is a non-invasive technique, which has been used in medicine and biomedical research since 1970. The MRI scan can show how the brain responds to different stimuli, enabling researchers to study both the functional and structural brain abnormalities in physiological disorders.
Functional MRI (fMRI) measures brain activity by detecting the changes in blood oxygenation and flow that occur in response to neural activity. The fMRI signal is not a direct measure of synaptic activities or action potential of cortical neurons. Instead, it results from the so-called blood-oxygen-leveldependent (BOLD) effect. An increase in neural activity in a cortical region increases local blood flow.
The fMRI data not only suggest an important role of the primary sensorimotor cortex in controlling motor actions but also indicate that the participation of multiple cortical areas may be essential for planning and executing a voluntary motor action. Therefore, brain imaging methods may be used to examine cortical representation and to predict clinical outcome and contribute to documenting the clinical outcome of the various treatments in a more ethology-based perspective.
An fMRI protocol has been tested for the first time for the short-time repeatability of patterns of brain activation provoked by bladder filling. The authors concluded that the technique provided a framework for comparing different fMRI protocols applied to bladder research .
The objective of this study was to identify studies which reported the brain activity measured by fMRI as a response to voluntary PFMs contractions and PFMT.
Materials & Methods
Electronic searches were performed of English literature with no preference of study design, Six digital databases (PubMed/MEDLINE, Embase, CINAHL, PEDro and Cochrane Library) were searched through the keywords “fMRI”, “voluntary pelvic floor muscle contractions”, “pelvic floor muscle”, “pelvic floor muscle training” and “pelvic floor muscle exercise”. In addition, articles in the reference lists of identified studies were hand searched.
Brain activity as a response to voluntary PFMs contractions (Table 1)
According to Fowler et al.  several neuroimaging studies in healthy adults have reported brain activities as response during PFMs contractions, although with divergent results [44-47]. Seseke et al. observed activity of the superolateral convexity of the semismooth cortex and the additional involuntary activity of the supplementary motor area (SMA) [46,47]. These divergent results of imaging studies have been explained by different PFMs exercises such as fast vs slow PFMs contractions. In contrast, Schrum et al. observed mostly activity in the SMA but without any differences between slow and fast PFMs contractions .
Seseke et al. measured the brain activity of voluntary PFMs contraction and relaxation in men by fMRI before and after prostatectomy.
In general, all participants had stronger activation during voluntary PFMs contractions than during relaxation in all regions before and after the prostatectomy .
Krhut et al. observed brain activity during bladder filling and by voluntary PFMs contractions in healthy females. The brain activity as a response to voluntary PFMs contractions was observed in the medial surface of the frontal lobe primary motor area (M1), bilaterally and left gyri’s pre-centralis .
Rana et al. reported that voluntary anal sphincter contractions have distinct brain networks to coordinate muscle synergies during functional tasks .
Yani et al. examine the degree to which the PFMs representation is described between SMA and the M1, and how this representation is utilized to activate the PFMs in different contraction patterns. The authors concluded that PFMs representation is broadly distributed in SMA and M1 in humans .
Furthermore, Seseke et al. demonstrated brain activity in dorsal/ventral part of PMC as a response to voluntary PFMs contractions and relaxation measured by fMRI in a rest model comparing healthy controls with patients with multiple sclerosis (MS) and clinically proven detrusor sphincter dyssynergia patients .
Groenendijk et al., newly demonstrated in a study of healthy males, that 7-tesla fMRI can be used to visualize the brain areas involved in pelvic floor control in the whole brain of the single subjects and define the specific brain areas involved in PFMs contraction. Before the scanning, the participants were instructed to perform correct voluntary PFMs contractions and during the scanning the participants performed a cycle of voluntary PFMs contractions in 21.5 s followed by 19.5 s in rest in a cycle repeated 12 times .
Brain activity as a response to PFMT (Table 2)
Di Gangi Herms et al. investigated the neuroplastic changes occurring after PFMT in female patients with stress urinary incontinence (SUI). The PFMT were with EMG-biofeedback, and the training was performed for 12 weeks. The results demonstrated after PFMT, more focused brain activity in M1 and the SMA. Significant activation was also found in the insula right frontal operculum and the anterior cingulate cortex, suggesting changes in emotional arousal in micturition after the PFMT .
These changes in the brain activity were related to clinical improvement documented by a decreased number of incontinence episodes and increased EMG-active of the PFMs after PFMT.
The changes in EMG-activity were also correlated with heightened BOLD responses in the M1 and primary sensory cortical representation sites of the lower urogenital tract .
The findings showed that PFMT with biofeedback might not only improve muscle strength and thereby support urethral support but also optimize central control of PFMs, bladder sensation as well as reflect the emotional neutralization related to symptom reduction.
Griffiths et al. aimed to investigate in a study the underlying mechanism of brain-bladder control and therapy during bladder filling .
A sample of women ≥ 60 years old with ≥ 5 urge urinary incontinence (UUI) episodes per week were chosen to give bio-feedback PFMT for 8-12 weeks. The participants underwent fMRI during provocation of urinary urgency before and after training, while normal controls were evaluated once for comparison. After PFMT a reduction of UI episodes (≥ 50%) was demonstrated in 28 (46%) responders. For the fMRI, two different patterns of brain reaction were demonstrated between responders and nonresponders. Moreover, the decrease cingulate activation appears to be a consequence of the improvement of UUI indicating by training while prefrontal deactivation may be a mechanism of contributing to the success of training . The authors concluded that in older women with UUI appears to be two patterns of brain reaction to bladder filling, and they seem to predict the response and nonresponse to bio-feedback assisted PFMT .
Based on these data reported by Griffiths et al. , Clarkson et al. supported the postulate, in secondary analysis, that responders and non-responders to therapy, may represent different subjects of UUI, one with more central aetiology and one without .
In the study by Griffiths et al. in older women with UUI and measured by fMRI, before and after PFMT, most neurological candidates were excluded. However, 7% to 9% of subjects in each subgroup had a history of a possible transient ischemic accident or mini-stroke without residual effect .
PFMT in neurological patients
Several studies in neurological patients with neurological diseases and NLUTD have reported a positive effect of PFMT. The diseases include MS [58-61], Parkinson’s disease (PD) [62,63], Spinal Cord Injury (SCI) [64,65] and Stroke [16-22,66,67]. However, no PFMT studies in neurological patients with NLUTD have used fMRI as an outcome measure to evaluate the effect.
In total, 14 studies were identified in this review. All the studies were published during 2005 - 2020. Of these, 12 studies reported data of brain activity as a response to voluntary PFMs contractions (Table 1) and two studies as a response to PFMT (Table 2).
|First author, year||Study sample (No)||Cortical region (main)|
|Zhang, 2005 ||Healthy adults (n=12)||2SMA, bilateral
|Seseke, 2006 ||Healthy female (n=11)||1PMC
|Kuhtz-Buschbeck, 2007 ||Healthy adults (n=30: 15females and 15 males)||2SMA
|Seseke, 2008 ||Healthy adults (n=23: 11females and 12 males)||1PMC
|Schrum, 2011 ||Healthy males (n=17)||2SMA
|Seseke, 2013 ||Males with clinical located prostate cancer (n=22)||1PMC
|Krhut, 2014 ||Healthy males (n=16)||4M1|
|Asavasopon, 2014 ||Healthy females (n=23)||4M1
|Rana, 2015 ||Healthy females (n=23)||4M1|
|Yani, 2018 ||no info||2SMA
|Seseke, 2019 ||Patients with MSi and detrusor sphincter dyssynergia (n=11: 8 females and 3 males)||Dorsal/ventral part of 1PMC|
|Groenendiik, 2020 ||Healthy males (n=17)||4M1
1PMC: Pontine micturition centre; 2SMA: Supplementary motor area; 3PAG: Periagueductal grey; 4M1: Primary motor cortex: 5MCG: Midcingulate gyrus; iMS: Multiple sclerosis.
Table 1: Studies reported brain activity as a response to voluntary pelvic floor muscle contractions measured by functional MRI.
|First author, year||Study sample (No)||Cortical region (main)|
|Di Gangi Herms, 2006 ||Females w. SUIa (n = 10)||4M1 2SMA|
|Griffiths, 2015 ||Older women w UUIb (n = 62)||Right ínsula medial Pre-frontal Cortex dorsal anterior cingulate córtex|
aSUI: Stress urinary incontinence; bUUI: Urge urinary incontinence; 2SMA: Supplementary motor area; 4M: Primary motor cortex
Table 2: Studies reported brain activity as a response to pelvic floor muscle training measured by functional MRI.
The participants (n=277) were of both genders and reasonably healthy adults (n=172, 62%), males with clinically diagnosed prostate cancer (n=22, 8%), females with stress urinary incontinence (n=10, 4%), older women with urge urinary incontinence (n=62, 22%), and patients with MS and detrusor sphincter dyssynergia (n=11, 4%), whereas no studies in stroke patients were identified.
The brain activity was broadly located to PMC, PAG, SMA, M1 and modelling supratemporal regions. The location of brain activity as a response to voluntary PFMs contractions are presented in Table 1 and for PFMT in Table 2.
In this review, published literature was investigated to identify studies which report brain activity measured by fMRI as a response to voluntary PFMs contractions and PFMT.
The identified studies were all recently published and occurred, in healthy adults or patients with voiding dysfunction. However, the identified studies focused primarily on the cerebral control of micturition circuit. At the same time, the brain activity as a response to voluntary PFMs contractions and PFMT measured by fMRI only played a role in the investigations.
In addition, even though there were many studies in neurologically patients with NLUTD which have reported a positive effect of PFMT, none of the studies have used fMRI as an outcome measure to evaluate the effect. Moreover, recently Harvie et al. identified in a metaanalysis, which regions in the brain were activated during the voiding phase of micturition, studies investigating PFMs contractions and studies with NLUTD were excluded .
The brain activity identified as a response to voluntary PFMs contractions and PFMT were broadly located to PMC, PAC, SMA, M1 and modelling supratemporal regions.
In addition, the motor system, studies using fMRI have consistently reported altered pattern of brain activity during activity or passive movement of a limb affected by stroke, compared with movements of healthy controls subjects .
Visualised changes in the brain activity as a response to PFMs contractions and PFMT measured by fMRI extend our knowledge to the underlying cortical processes and mechanism of the treatment in patients with voiding dysfunction, particularly if there are correlations between neuroimage observations and clinical data. In a study by Seseke et al. a higher level of brain activity measured by fMRI was reported even before and after prostatectomy in men diagnosed with clinical prostate cancer, when the participants performed PFMs contractions to mimic voiding compere to PFMs relaxation to mimic voiding . This result supports the positive clinical results in a randomised controlled trial (RCT) by Tibaek et al. Evaluating the effect of PFMT before transurethral resection of the prostate (TURP) .
PFMT is a non-invasive treatment with no reported adverse effects. By the fMRI, as an outcome measure opens new possibilities for the goal to improve not only muscular strength-enhancing support of the urethra but also optimized cerebral muscular control of the PFMS, modulate bladder sensation as well as reflect the emotional neutralisation related to symptom reaction .
Cramer et al. reported, in a study of healthy controls and measured by fMRI, that there is a relationship between different squeezing force and neuronal firing rate in motor cortex activation . Likewise, Dai et al. demonstrated relationship between muscle force measured by surface EMG and brain activation measured by fMRI . In the study by Dai et al. handgrip was used performing the voluntary force. Thus, studies investing the relationship between different force levels of the voluntary PFMs contractions and brain activity are still lacked.
Several questions still need to be explored, such as: “Does the voluntary PFMs contractions and PFMT have an inhibitory effect on the overactive detrusor?”; “Does a change of BOLD associated with increased PFMs function?” and “To which extent can the brain structures predict how well an individual will learn a motor task as a response to specific therapies?”.
According to Clarkson et al. the analysis of fMRI data among groups of subjects yields valuable insight in the bladder control, mechanisms whereas the fMRI is not yet appropriate for evaluation of brain’s role in continence on an individual level . Hence, according to Khavari et al., both data from clinical outcome measures and neuroimage outcome measures as fMRI must be applied as documentation in current and future studies focusing patients with voiding dysfunction .
This study involved several limitations.
First, the lack of statistical calculations based on the limited available data and the heterogeneous characteristics of patients.
Second, the lack of consistency in the used methods in the fMRI studies .
In a study by Kutch et al. focusing on brain structure and function for patients with Urologic Chronic Pelvic Syndrome, fMRI data were used and analysed from, the Multidisciplinary Approach to the Study of Chronic Pelvic Pain (MAPP) Research Network because of the limitations of previous studies . The MAPP Study protocol provides both baseline and longitudinal data allocated of a large cohort of patients and controls . A similar approach might be considered, focusing on brain structures and function for patients with NLUTD treated with PFMT, to improve the evidence-base for development for future clinical studies, and ultimately, improving clinical management.
Patients with voiding dysfunction need proper diagnosis and treatment.
If brain activity as a response to PFMT positively effects bladder control perform increases and decreases effects on bladder control, we take a step towards understanding underlying mechanisms and its treatment effect. The next step must be to investigate brain activity as a response to voluntary PFMs contractions and PFMT measured by fMRI in large, homogenous groups and subgroups of patients with voiding dysfunction, particularly stroke patients with NLUTD where there is clearly a gap in knowledge.
We expect that the present study can serve as a basis for further investigations whether interventions like PFMT have an impact on cortical and subcortical activation patterns.
This review identified studies which indicate that fMRI even provide valuable outcome data supporting clinical outcome data and provide knowledge of the underlying neurophysiological mechanisms in the brain and its control of the bladder by voluntary PFMs contractions and PFMT. The findings underline needs for studies using fMRI as an outcome measurement in large homogenous groups and subgroups of patients with voiding dysfunction. In particular, there is a call for studies providing knowledge of brain activity as response to voluntary PFMs contractions and PFMT in stroke patients with NLUTD
Conflicts of Interest
The author reports no conflicts of interest.
This study was funded by the Department of Occupational Therapy and Physiotherapy, Rigshospitalet Glostrup, Copenhagen University Hospital, Denmark.
2. Nakayama H, Jørgensen HS, Pedersen PM, Raaschou HO, Olsen TS. Prevalence and risk factors of incontinence after stroke: the Copenhagen Stroke Study. Stroke. 1997 Jan;28(1):58-62.
3. Brittain KR, Peet SM, Castleden CM. Stroke and incontinence. Stroke. 1998 Feb;29(2):524-8.
4. Jørgensen L, Engstad T, Jacobsen BK. Self-reported urinary incontinence in noninstitutionalized long-term stroke survivors: A population-based study. Archives of Physical Medicine and Rehabilitation. 2005 Mar 1;86(3):416-20.
5. Kolominsky-Rabas PL, Hilz MJ, Neundoerfer B, Heuschmann PU. Impact of urinary incontinence after stroke: results from a prospective populationbased stroke register. Neurourology and Urodynamics: Official Journal of the International Continence Society. 2003;22(4):322-7.
6. Tibaek S, Gard G, Klarskov P, Iversen HK, Dehlendorff C, Jensen R. Prevalence of lower urinary tract symptoms (LUTS) in stroke patients: a cross-sectional, clinical survey. Neurourology and Urodynamics: Official Journal of the International Continence Society. 2008 Nov;27(8):763-71.
7. Chung JH, Kim JB, Kim JH. Lower urinary tract symptoms in male patients with stroke: A nationwide population-based study. Archives of Gerontology and Geriatrics. 2019 Jul 1;83:309-14.
8. Brittain KR, Shaw C. The social consequences of living with and dealing with incontinence—A carers perspective. Social Science & Medicine. 2007 Sep 1;65(6):1274-83.
9. Itoh Y, Yamada S, Konoeda F, Koizumi K, Nagata H, Oya M, et al. Burden of overactive bladder symptom on quality of life in stroke patients. Neurourology and Urodynamics. 2013 Jun;32(5):428-34.
10. Groen J, Pannek J, Diaz DC, Del Popolo G, Gross T, Hamid R, Karsenty G, Kessler TM, Schneider M, Blok B. Summary of European Association of Urology (EAU) guidelines on neuro-urology. European Urology. 2016 Feb 1;69(2):324-33.
11. Gormley EA, Lightner DJ, Burgio KL, Chai TC, Clemens JQ, Culkin DJ, Das AK, Foster HE, Scarpero HM, Tessier CD, Vasavada SP. Diagnosis and treatment of overactive bladder (non-neurogenic) in adults: AUA/SUFU guideline. The Journal of Urology. 2012 Dec;188(6S):2455-63.
12. Hay-Smith J, Berghmans B, Burgio KL. Adult conservative management: Committee 12. Health Publication Ltd. 2009 P.1025-1108.
13. Hunter KF, Moore KN, Glazener CM. Conservative management for postprostatectomy urinary incontinence. Cochrane Database of Systematic Reviews. 2007(2).
14. Newman DK, Guzzo T, Lee D, Jayadevappa R. An evidence-based strategy for the conservative management of the male patient with incontinence. Current Opinion in Urology. 2014 Nov 1;24(6):553-9.
15. Dumoulin C, Cacciari LP, Hay-Smith EJ. Pelvic floor muscle training versus no treatment, or inactive control treatments, for urinary incontinence in women. Cochrane database of systematic reviews. 2018(10).
16. Tibaek S, Gard G, Jensen R. Pelvic floor muscle training is effective in women with urinary incontinence after stroke: a randomised, controlled and blinded study. Neurourology and Urodynamics: Official Journal of the International Continence Society. 2005;24(4):348-57.
17. 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?. International Urogynecology Journal. 2007 Mar 1;18(3):281-7.
18. Tibaek S, Gard G, Dehlendorff C, Iversen HK, Biering-Soerensen F, Jensen R. Is pelvic floor muscle training effective for men with poststroke lower urinary tract symptoms? a single-blinded randomized, controlled trial. American journal of men’s health. 2017 Sep;11(5):1460-71.
19. Arkan G, Beser A, Ozturk V, Bozkurt O, Gulbahar S. Effects on urinary outcome of patients and caregivers’ burden of pelvic floor muscle exercises based on the health belief model done at home by post-stroke patients. Topics in stroke rehabilitation. 2019 Feb 17;26(2):128-35.
20. Shin DC, Shin SH, Lee MM, Lee KJ, Song CH. Pelvic floor muscle training for urinary incontinence in female stroke patients: a randomized, controlled and blinded trial. Clinical rehabilitation. 2016 Mar;30(3):259-67.
21. Tibæk S, Gard G, Dehlendorff C, Iversen HK, Erdal J, Biering-Sørensen F, et al. The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke. Topics in Stroke Rehabilitation. 2015 Jun 1;22(3):185-93.
22. Tibaek S, Gard G, Dehlendorff C, Iversen H, Biering- Soerensen F, Jensen R. Can pelvic floor muscle training improve quality of life in men with mild to moderate poststroke and lower urinary tract symptoms? A randomised, controlled and single-blinded trial. Eur J Phys Rehabil Med. 2016 Mar 22;53:416-25.
23. Bernstein IT. The pelvic floor muscles: Muscle thickness in healthy and urinary-incontinent women measured by perineal ultrasonography with reference to the effect of pelvic floor training. Estrogen receptor studies. Neurourology and Urodynamics: Official Journal of the International Continence Society. 1997;16(4):237-75.
24. Lukacz ES, Lawrence JM, Contreras R, Nager CW, Luber KM. Parity, mode of delivery, and pelvic floor disorders. Obstetrics & Gynecology. 2006 Jun 1;107(6):1253-60.
25. Handa VL, Blomquist JL, Knoepp LR, Hoskey KA, McDermott KC, Muñoz A. Pelvic floor disorders 5-10 years after vaginal or cesarean childbirth. Obstetrics and Gynecology. 2011 Oct;118(4):777.
26. Memon HU, Handa VL. Vaginal childbirth and pelvic floor disorders. Women’s health. 2013 May;9(3):265-77.
27. Peng Y, Miller BD, Boone TB, Zhang Y. Modern theories of pelvic floor support. Current Urology Reports. 2018 Jan 1;19(1):9.
28. Critchley HO, Dixon JS, Gosling JA. Comparative study of the periurethral and perianal parts of the human levator ani muscle. Urologia Internationalis. 1980;35(3):226-32.
29. Gilpin SA, Gosling JA, Smith AR, Warrell DW. The pathogenesis of genitourinary prolapse and stress incontinence of urine. A histological and histochemical study. BJOG: An International Journal of Obstetrics & Gynaecology. 1989 Jan;96(1):15-23.
30. Gosling JA, Dixon JS, Critchley HO, THOMPSON SA. A comparative study of the human external sphincter and periurethral levator ani muscles. British Journal of Urology. 1981 Feb;53(1):35-41.
31. Dixon JS, Gosling JA. Histomorphology of the pelvic floor. Springer Verlag. 1994 p. 28-33.
32. Fowler CJ. Neurological disorders of micturition and their treatment. Brain. 1999 Jul 1;122(7):1213-31.
33. Bø K, Hagen RH, Kvarstein B, Jørgensen J, Larsen S, Burgio KL. Pelvic floor muscle exercise for the treatment of female stress urinary incontinence: III. Effects of two different degrees of pelvic floor muscle exercises. Neurourology and Urodynamics. 1990;9(5):489-502.
34. Eisner-Janowicz I, Barbay S, Hoover E, Stowe AM, Frost SB, Plautz EJ, Nudo RJ. Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. Journal of Neurophysiology. 2008 Sep;100(3):1498-512.
35. Nudo RJ, Milliken GW. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. Journal of Neurophysiology. 1996 May 1;75(5):2144-9.
36. Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. Journal of Neurophysiology. 2003 Jun;89(6):3205-14.
37. Rossini PM, Calautti C, Pauri F, Baron JC. Poststroke plastic reorganisation in the adult brain. The Lancet Neurology. 2003 Aug 1;2(8):493-502.
38. Biernaskie J, Chernenko G, Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. Journal of Neuroscience. 2004 Feb 4;24(5):1245-54.
39. Verheyden G, Nieuwboer A, De Wit L, Thijs V, Dobbelaere J, Devos H, et al. Time course of trunk, arm, leg, and functional recovery after ischemic stroke. Neurorehabilitation and Neural Repair. 2008 Mar;22(2):173-9.
40. Askim T, Indredavik B, Vangberg T, Håberg A. Motor network changes associated with successful motor skill relearning after acute ischemic stroke: a longitudinal functional magnetic resonance imaging study. Neurorehabilitation and Neural Repair. 2009 Mar;23(3):295-304.
41. Favre I, Zeffiro TA, Detante O, Krainik A, Hommel M, Jaillard A. Upper limb recovery after stroke is associated with ipsilesional primary motor cortical activity: a meta-analysis. Stroke. 2014 Apr;45(4):1077- 83.
42. Clarkson BD, Tyagi S, Griffiths DJ, Resnick NM. Test-retest repeatability of patterns of brain activation provoked by bladder filling. Neurourology and Urodynamics. 2017 Aug;36(6):1472-8.
43. Fowler CJ, Griffiths DJ. A decade of functional brain imaging applied to bladder control. Neurourology and Urodynamics: Official Journal of the International Continence Society. 2010 Jan;29(1):49-55.
44. Zhang H, Reitz A, Kollias S, Summers P, Curt A, Schurch B. An fMRI study of the role of suprapontine brain structures in the voluntary voiding control induced by pelvic floor contraction. Neuroimage. 2005 Jan 1;24(1):174-80.
45. Kuhtz-Buschbeck JP, Van der Horst C, Wolff S, Filippow N, Nabavi A, Jansen O, Braun PM. Activation of the supplementary motor area (SMA) during voluntary pelvic floor muscle contractions—an fMRI study. Neuroimage. 2007 Apr 1;35(2):449-57.
46. Seseke S, Baudewig J, Kallenberg K, Ringert RH, Seseke F, Dechent P. Gender differences in voluntary micturition control—An fMRI study. Neuroimage. 2008 Nov 1;43(2):183-91.
47. Seseke S, Baudewig J, Kallenberg K, Ringert RH, Seseke F, Dechent P. Voluntary pelvic floor muscle control—an fMRI study. Neuroimage. 2006 Jul 15;31(4):1399-407.
48. Schrum A, Wolff S, Van der Horst C, Kuhtz-Buschbeck JP. Motor cortical representation of the pelvic floor muscles. The Journal of Urology. 2011 Jul;186(1):185-90.
49. Seseke S, Baudewig J, Ringert RH, Rebmann U, Dechent P. Monitoring brain activation changes in the early postoperative period after radical prostatectomy using fMRI. Neuroimage. 2013 Sep 1;78:1-6.
50. Krhut J, Holy P, Tintera J, Zachoval R, Zvara P. Brain activity during bladder filling and pelvic floor muscle contractions: a study using functional magnetic resonance imaging and synchronous urodynamics. International Journal of Urology. 2014 Feb;21(2):169-74.
51. Rana M, Yani MS, Asavasopon S, Fisher BE, Kutch JJ. Brain connectivity associated with muscle synergies in humans. Journal of Neuroscience. 2015 Nov 4;35(44):14708-16.
52. Yani MS, Wondolowski JH, Eckel SP, Kulig K, Fisher BE, Gordon JE, Kutch JJ. Distributed representation of pelvic floor muscles in human motor cortex. Scientific reports. 2018 May 8;8(1):1-6.
53. Seseke S, Leitsmann C, Hijazi S, Trojan L, Dechent P. Functional MRI in patients with detrusor sphincter dyssynergia: Is the neural circuit affected?. Neurourology and Urodynamics. 2019 Nov;38(8):2104-11.
54. Groenendijk IM, Luijten SP, de Zeeuw CI, Holstege JC, Scheepe JR, van der Zwaag W, Blok BF. Whole brain 7T-fMRI during pelvic floor muscle contraction in male subjects. Neurourology and Urodynamics. 2019 Nov 13.
55. Herms AD, Veit R, Reisenauer C, Herms A, Grodd W, Enck P, Stenzl A, Birbaumer N. Functional imaging of stress urinary incontinence. Neuroimage. 2006 Jan 1;29(1):267-75.
56. Griffiths D, Clarkson B, Tadic SD, Resnick NM. Brain mechanisms underlying urge incontinence and its response to pelvic floor muscle training. The Journal of Urology. 2015 Sep;194(3):708-15.
57. Clarkson BD, Karim HT, Griffiths DJ, Resnick NM. Functional connectivity of the brain in older women with urgency urinary incontinence. Neurourology and Urodynamics. 2018 Nov;37(8):2763-75.
58. McClurg D, Ashe RG, Marshall K, Lowe-Strong AS. Comparison of pelvic floor muscle training, electromyography biofeedback, and neuromuscular electrical stimulation for bladder dysfunction in people with multiple sclerosis: a randomized pilot study. Neurourology and Urodynamics: Official Journal of the International Continence Society. 2006;25(4):337-48.
59. Lúcio A, D’ancona CA, Perissinotto MC, McLean L, Damasceno BP, de Moraes Lopes MH. Pelvic floor muscle training with and without electrical stimulation in the treatment of lower urinary tract symptoms in women with multiple sclerosis. Journal of Wound Ostomy & Continence Nursing. 2016 Jul 1;43(4):414-9.
60. Lúcio AC, D’Ancona CA, Lopes MH, Perissinotto MC, Damasceno BP. The effect of pelvic floor muscle training alone or in combination with electrostimulation in the treatment of sexual dysfunction in women with multiple sclerosis. Multiple Sclerosis Journal. 2014 Nov;20(13):1761-8.
61. Lucio AC, Perissinoto MC, Natalin RA, Prudente A, Damasceno BP, D’ancona CA. A comparative study of pelvic floor muscle training in women with multiple sclerosis: its impact on lower urinary tract symptoms and quality of life. Clinics. 2011;66(9):1563-8.
62. Vaughan CP, Burgio KL, Goode PS, Juncos JL, McGwin G, Muirhead L, Markland AD, Johnson TM. Behavioral therapy for urinary symptoms in Parkinson’s disease: A randomized clinical trial. Neurourology and Urodynamics. 2019 Aug;38(6):1737-44.
63. Vaughan CP, Juncos JL, Burgio KL, Goode PS, Wolf RA, Johnson TM. Behavioral therapy to treat urinary incontinence in Parkinson disease. Neurology. 2011 May 10;76(19):1631-4.
64. Vasquez, N., et al., Pelvic floor muscle training in spinal cord injury and its impact on neurogenic detrusor over-activity and incontinence. Spinal Cord, 2015. 53(12): p. 887-9.
65. Elmelund M, Biering-Sørensen 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 investigatorblinded parallel randomized clinical trial. International Urogynecology Journal. 2018 Nov 1;29(11):1597-606.
66. 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 randomised, controlled and blinded study. International Urogynecology Journal. 2004 Apr 1;15(2):117-23.
67. Thomas LH, Coupe J, Cross LD, Tan AL, Watkins CL. Interventions for treating urinary incontinence after stroke in adults. Cochrane Database of Systematic Reviews. 2019(2).
68. Khavari R, Boone TB. Functional Brain Imaging in Voiding Dysfunction. Current Bladder Dysfunction Reports. 2019 Mar 15;14(1):24-30.
69. Cao Y, D’olhaberriague L, Vikingstad EM, Levine SR, Welch KM. Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis. Stroke. 1998 Jan;29(1):112-22.
70. Tibaek S, Klarskov P, Lund Hansen B, Thomsen H, Andresen H, Schmidt Jensen C, Niemann Olsen M. Pelvic floor muscle training before transurethral resection of the prostate: a randomized, controlled, blinded study. Scandinavian Journal of Urology and Nephrology. 2007 Jan 1;41(4):329-34.
71. Cramer SC, Weisskoff RM, Schaechter JD, Nelles G, Foley M, Finklestein SP, Rosen BR. Motor cortex activation is related to force of squeezing. Human brain mapping. 2002 Aug;16(4):197-205.
72. Dai TH, Liu JZ, Sahgal V, Brown RW, Yue GH. Relationship between muscle output and functional MRI-measured brain activation. Experimental Brain Research. 2001 Oct 1;140(3):290-300.
73. Shafik A, Shafik IA. Overactive bladder inhibition in response to pelvic floor muscle exercises. World Journal of Urology. 2003 May 1;20(6):374-7.
74. Guo Q, Parlar M, Truong W, Hall G, Thabane L, McKinnon M, Goeree R, Pullenayegum E. The reporting of observational clinical functional magnetic resonance imaging studies: a systematic review. PloS one. 2014;9(4).
75. Kutch JJ, Ichesco E, Hampson JP, Labus JS, Farmer MA, Martucci KT, Ness TJ, Deutsch G, Apkarian AV, Mackey SC, Klumpp DJ. Brain signature and functional impact of centralized pain: a multidisciplinary approach to the study of chronic pelvic pain (MAPP) network study. Pain. 2017 Oct;158(10):1979.
76. Asavasopon S, Rana M, Kirages DJ, Yani MS, Fisher BE, Hwang DH, Lohman EB, Berk LS, Kutch JJ. Cortical activation associated with muscle synergies of the human male pelvic floor. Journal of Neuroscience. 2014 Oct 8;34(41):13811-8.