Topics in Stroke Rehabilitation
ISSN: 1074-9357 (Print) 1945-5119 (Online) Journal homepage: http://www.tandfonline.com/loi/ytsr20
The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke S. Tibaek, G. Gard, C. Dehlendorff, H. K. Iversen, J. Erdal, F. Biering-Sørensen, G. Dorey & R. Jensen To cite this article: S. Tibaek, G. Gard, C. Dehlendorff, H. K. Iversen, J. Erdal, F. BieringSørensen, G. Dorey & R. Jensen (2015) The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke, Topics in Stroke Rehabilitation, 22:3, 185-193, DOI: 10.1179/1074935714Z.0000000019 To link to this article: http://dx.doi.org/10.1179/1074935714Z.0000000019
Published online: 17 Mar 2015.
Submit your article to this journal
Article views: 59
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ytsr20 Download by: [University of Waterloo]
Date: 12 November 2016, At: 19:46
The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke S. Tibaek1, G. Gard2, C. Dehlendorff3, H. K. Iversen4, J. Erdal5, F. Biering-Sørensen6, G. Dorey7, R. Jensen4 1
Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen, Glostrup, Denmark, 2Department of Health Sciences, Division of Physiotherapy, Lund University, Lund, Sweden, 3 Danish Cancer Society Research Centre, Danish Cancer Society, Copenhagen, Denmark, 4Department of Neurology, Glostrup Hospital, University of Copenhagen, Denmark, 5Department of Neurology, Herlev Hospital, University of Copenhagen, Herlev, Denmark, 6Department of Spinal Cord Injuries, Glostrup Hospital, University of Copenhagen, Glostrup, Denmark, 7Department of Health and Applied Sciences, University of the West of England, Bristol, UK Background: Erectile dysfunction and lower urinary tract symptoms (LUTS) are common sequelae in men after stroke. Objective: The objective of this study was to evaluate the effect of pelvic floor muscle training (PFMT) on measured erectile function as an indicator of sexuality in men with LUTS after stroke. Method: A sample of 516 men with stroke was invited to participate in this single-blinded, randomized controlled trial according to in- and exclusion criteria. This resulted in 31 participants who were randomized to either a Treatment Group (n516) or a Control Group (n515). The intervention included 12weeks of PFMT. The effect was measured on the International Index of Erectile Function (IIEF-5) questionnaire. Results: Thirty participants (median age: 68 years; interquartile range: 60–74 years) completed the study, 15 in each group. The results of the IIEF-5 sum score showed a significant improvement (Pv0.04) from pre-test to post-test in the Treatment Group, but not in the Control Group. Within pre-test and 6-month follow-up, the median sum score decreased in both groups, worsened in the Control Group [Treatment Group, 3 (17%) versus Control Group, 5 (31%)]. There were differences between the groups at post-test and at follow-up, but they were not statistically significant. Conclusion: The results showed that, as measured by erectile function in men with LUTS after stroke, PFMT may have short-term and long-term effect, although no statistically significant effect was demonstrated between the groups. Keywords: Erectile function, LUTS, Men, Pelvic floor muscle training, Stroke
Introduction Erectile dysfunction (ED) is highly prevalent in men after stroke, ranging from 48 to 62%.1,2 However, it is seldom a consequence of stroke alone; physical and cognitive deficits, depression and lower urinary tract symptoms (LUTS)3 are likely to contribute. ED as an aspect of sexuality is an integral and important part of quality of life in men with stroke4–6 as it is for their partners.7 Particularly for stroke patients with LUTS, urinary incontinence during sexual activity can be challenging.
Correspondence to: S. Tibaek, Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen, Ndr. Ringvej 57, 2600, Glostrup, Denmark. Email: [email protected] ß W. S. Maney & Son Ltd 2015
DOI 10.1179/1074935714Z.0000000019
ED is defined as the consistent or recurrent inability of a man to obtain and/or maintain a penile erection sufficient for sexual performance.8 Erection requires intact vascular and neural functions and ED is linked to aging and a variety of co-existing medical conditions (hypertension, diabetes, cardiovascular disease, and LUTS).9,10 In addition, many of the antihypertensive agents commonly used by stroke patients may impair erection due to a concomitant lowering of the cavernosal arterial pressure; some (such as beta blockers) may also reduce sexual desire.4 The erectile blood flow, controlled by the autonomic erection centers, provides parasympathetic (S2–S4) and sympathetic (T12–L2) innervations to the pelvic plexus, which include the cavernous nerve Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
185
Tibaek et al.
The effect of PFMT in stroke
that innervate the cavernosal arteries and trabecular smooth muscle. The somatic motor nerve supply arises from the sacral spinal cord and innervates through the pudendal nerve the bulbocavernosus and ischiocavernosus muscles, which are active during ejaculation and climax.11 Treatment of ED in neurologically healthy men usually consists of pharmacotherapy,11,12 whereas there is little information on ED treatment in stroke patients.9,13 Physical activity has been shown to reduce the risk of ED14,15 and as measured by improvement in erection function score,6 may even reverse its development. Moreover, Kratzik et al. showed that physical exercise had a positive impact on men with ED.16 Pelvic floor muscle training (PFMT) has been shown to be effective on prostate pre- and postsurgical LUTS.17,18 Moreover, it was also found to have a significant effect in otherwise healthy men with ED19–21 measured by the International Index of Erectile Function (IIEF).22 Previously, PFMT has been shown to have a significant effect on urinary incontinence in women after stroke.23 Although ED and LUTS are highly prevalent in men with stroke and PFMT is effective in neurologically healthy men with ED and LUTS, we were not able to find published research data on the effect of PFMT in male stroke patients with ED and LUTS. The purpose of this study was to evaluate the effect of PFMT measured on erectile function as an indicator of sexuality in men with LUTS after stroke.
Methods This study is part of a large, multifaceted study focusing on PFMT in men with LUTS after stroke.
Participants Between 1 February 2010 and 31 December 2012, medical records of men with stroke from the Departments of Neurology, Glostrup and Herlev Hospitals, University of Copenhagen were successively screened by the project leader (ST) for inclusion according to the following inclusion and exclusion criteria. Inclusion criteria: (1) men diagnosed with stroke clinically according to the World Health Organization definition24 and/or confirmed by computer tomography or magnetic resonance scan; (2) at least 1 month since last stroke; (3) normal cognitive function (minimal mental examination score w25);25 (4) LUTS according to the International Continence Society definition,26 with start or aggravation close in time to the stroke and measured by the Danish Prostatic Symptoms Score (DAN-PSS-1) Questionnaire;27 186
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
(5) ability to walk independently indoors for at least 100m with or without walking aids; (6) ability to visit toilet independently; and (7) age w18years. Exclusion criteria: (1) prior history of LUTS surgery, pelvic surgery, or trauma; (2) more than two diagnosed strokes; (3) other severe neurological disease including dementia; (4) severe dysphasia; (5) severe psychiatric disease; (6) prostate cancer; and (7) inability to speak Danish or English. Demographic, neurological, urological, and physical baseline characteristics were obtained from the medical records and at the first study consultation.
Design The design was a prospective randomized, controlled and single-blinded, parallel group trial (RCT). A 4-week run-in period including an initial investigation sequence (pre-test) was followed by randomization to either a Treatment Group (TG) or a Control Group (CG). After 12weeks, the second investigation sequence was performed (post-test), with the final investigation sequence (follow-up) after further 6 months. Randomization was based on a mathematical table, delivered in blocks of 10 in sealed envelopes and managed by a person who did not participate further in the study. Registration of variables from the pre-test, posttest, and follow-up investigations sequences were managed by individuals (physiotherapists) who were blinded to the randomization code of the participants, while the physiotherapist treating the participants with PFMT was unblinded. The participants randomized for CG were all offered a 12-week PFMT program after the trial. The participants received verbal and written information and signed an informed consent before study entry. The study was approved by the Ethical Committee of Copenhagen Capital Registration (H-B-2009-069) and registered in the Danish Register for Data protection and in Clinical Trials.gov Protocol Registration System (Clinical Trials NTC01042249).
Intervention All the same, specialized physiotherapist, in a systematic, controlled, intensive PFMT program over 12 consecutive weeks, treated the participants in the TG. The procedure is presented in Table 1. The content of the treatment program: 1. Introduction (theory): information about prevalence and definition of LUTS, anatomy and physiology of the bladder and the pelvic floor muscle (PFM), motivation and instruction in home exercises. 2. Home exercises: PFM strengthening exercise by performing close to maximum contraction (6-second contraction/6-second rest);28 endurance
Tibaek et al.
Table 1 Pelvic floor muscle training program for men with stroke Introduction (theory)
60minutes
Group treatment Frequency
3–6 participants/group 1 session (60minutes) per week 12weeks i8 sessions
Duration Attendance in group -treatment sessions Digital anal palpation Home exercises
2–3 times 1–2 times daily
PFM exercise by performing sub-maximal contraction for as long as possible (max 30-second contraction/30-second rest). Participants were instructed to repeat the exercise program gradually 6–10 times in supine, standing and sitting positions, once or twice daily. 3. Group treatments consist of isolated PFM contraction (6-second contraction/6-second rest); strength exercises (3-second contraction/3-second rest, and 6-second contraction/6-second rest); endurance exercises (max 30-second sub-maximal contraction/ 30-second rest). Sub-maximal PFM contractions before and during coughing, sneezing, laughing, and in daily activities such as rising, sitting, and lifting. 4. All techniques were repeated 4–8 times in supine, standing and sitting positions, and during activates such as: slow and fast walking. 5. Digital anal palpation of PFM was performed to control correct contraction, to give continual feedback to the participants, and to evaluate the PFM strength. The participants in TG received only feedback at digital anal palpation 2–3 times.
The training program was a modified version of a standard program for group treatment of stress incontinence.23,29 The participants in the CG followed the normal, standard program of general rehabilitation without specific treatment for LUTS.
Main outcome measures The effect of PFMT was measured on the IIEF-5 questionnaire.22 The IIEF-5 assesses the prevalence and severity of ED according to the classification system developed by Rosen et al.22 It consists of five questions each scored from 0 to 5. Question number 1 addresses confidence in the erectile function, questions 2–4 the actual erectile function capacity, and question number 5 intercourse satisfaction. The IIEF-5 sum score is the sum of the ordinal responses to the five questions. The severity levels are classified for the sum score 22–255no ED, for 17–215mild ED, for 12–165mild to moderate ED, for 8–115moderate ED, and for 1–75severe ED.22 The IIEF-5 is a patient-administered questionnaire.
The effect of PFMT in stroke
In this study, the participants were asked to fill in the IIEF-5 based on the previous month in contrast to 3months in the original version.
Additional question The questionnaire included the following EDinduced bother question A1 ‘‘If you were to spend the rest of your life with your ED problems as they are now, how would you feel about that?’’ The answer was rated on an ordinal scale (1–5) (15very dissatisfied, 25some dissatisfaction, 35neither satisfied nor dissatisfied, 45some satisfaction, 55very satisfied).30 Followed by A2: ‘‘If you use medicine or other aids/appliances to optimize erection, is that reflected in your answer in question A1?’’ The answer was rated on a binominal scale (with, or without, medicine or aids/appliance).
Statistical analysis Statistical analyses were carried out using IBM SPSS (Statistical Package of Social Science) version 20. and R, version 2.5.0.31 Median and interquartile range are presented for small samples. The null-hypothesis between groups was tested by the Mann–Whitney U test and within groups using Wilcoxon signed rank test. For all tests, the level for statistical significant was set to Pv0.05. Power calculations showed that, with 90% power (beta50.9) and a significance level at P50.05, a total of 120 participants were needed for the study.
Results Participants Medical records of 1812 men with stroke were screened for inclusion and 516 were invited to participate in this RCT. Of these, 62 (12%) did not respond, 241 (47%) reported that they did not have any LUTS, while 113 (22%) had LUTS before the stroke and its status was unchanged, 13 (2%) had LUTS related to a history of prostate surgery but not noted in their medical records, 51 (10%) had LUTS, but no resources to participate or did not want to do so, leaving 36 (7%) for inclusion. However, five of these men did not show up for inclusion and pre-test (n51: ‘‘too much hospital’’; n54: no information), leaving 31 for inclusion. After the first investigation, sequence one participant (randomized to the TG) dropped out (unknown reason) before starting the PFMT sessions. The remaining 30 participants, 15 in each group, with a median age of 68 (interquartile range 60–74), completed the study. At follow-up, one participant from the CG was lost for follow-up. The trial had to be closed after 35months due to poor recruitment of participants. Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
187
Tibaek et al.
The effect of PFMT in stroke
Median PFMT session attendance rate in TG was 11 (interquartile range: 10–12), corresponding to 92%.
Characteristics Demographic baseline characteristics of the study group are presented in Table 2. Neurological, urological, and physical baseline characteristics are presented in Table 3. There were no significant differences between the TG and the CG for any baseline characteristics.
IIEF-5 The median IIEF-5 sum score at baseline was 17 (interquartile range: 5–23). The results (Table 4) showed a significant improvement in the TG from pre-test to post-test, but not in the CG. There were no statistical significant differences between TG and CG either at pre-test or at post-test (Fig. 1).
At 6-month follow-up, the results showed no significant difference between groups or within groups (pre-test versus follow-up). However, IIEF-5 sum scores within pre-test and follow-up were worsened in the CG (Table 4, Fig. 1). Data were missing in the TG (n52, 13%) and in the CG (n57–9, 47–60%). Six participants reported that they were not sexually active. Moreover, 3–5 participants failed to complete at least one out of five questions in the IIEF-5 questionnaire at pre-test, post-test, or follow-up, respectively, which made it impossible to calculate the IIEF-5 sum scores. The proportion of answering was as following: TG: pre-test587%; post-test587%; follow-up587% versus CG: pre-test547%; post-test564%; followup540%.
Table 2 Demographic baseline characteristics of men with stroke in the trial Treatment Group Characteristic Age, yearsa Past medical history, diseases and risk factors Stroke (one attack) Hypertension Transient ischemic attack Diabetes mellitus Coronary heart disease Other diseases (arthritis, fractures, muscular disorders, etc.) None Smoking Smoker Former smoker Never smoked No information Alcohol, no. consumed units per week 0 0–6 7–13 14–21 w21 No information Social status Employed Unemployed Early retired/sick leave w3months Retired No information Civil status Single/divorced Married/partnered Widower No information Current use of medication Antiarrhythnics/antihypertensives Statins Anticoagulants/antithrombotics Hypoglycaenics agents Analgesics Antidepressants Other No medicine Note: aMedian (interquartile range).
188
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
n515 No. (%) 68 (57–73) 0 4 0 2 3 5 7
(0) (27) (0) (13) (20) (33) (47)
2 (13) 3 (20) 10 (67) 0 (0) 5 5 2 2 1 0
(33) (33) (13) (13) (7) (0)
Control Group n515 No. (%) 70 (64–75) 5 5 1 1 0 5 2
P value 0.22
(33) (33) (7) (7) (0) (33) (13)
0.13 0.78 0.78 0.78 0.37 1.00 0.13
2 (13) 1 (7) 12 (80) 0 (0)
0.49
7 6 1 0 1 0
(47) (40) (7) (0) (7) (0)
0.33
5 (33) 0 (0) 1 (7) 9 (60) 0 (0)
2 (13) 0 (0) 3 (20) 10 (67) 0 (0)
0.57 -
4 (27) 10 (67) 1 (7) 0 (0)
4 (27) 11 (73) 0 (0) 0 (0)
0.84
10 (67%) 12 (80%) 12 (80%) 1 (7%) 1 (7%) 1 (7%) 5 (33%) 0 (0%)
6 (40%) 10 (67%) 12 (80%) 0 (0%) 1 (7%) 0 (0%) 7 (47%) 0 (0%)
0.22 0.54 1,00 0,77 1.00 0.77 0.54 1.00
Tibaek et al.
The effect of PFMT in stroke
Table 3 Neurological, urological, and physical baseline characteristics of men with stroke Treatment Group Characteristic Neurological a Mini-mental state examination score (maximum score530) a Barthel Index (maximum score5100) 38 a Time since last stroke, days Result of stroke verification by CT or MRI scan Visible stroke at imaging No visible stroke at imaging, but clinical stroke Subtypes of stroke Infarct Hemorrhage Infarctzhemorrhage No infarct No information Localisation Left hemisphere Right hemisphere Bilateral Unclassified No information Urological c Past history of LUTS None Pharmacological treatment No information Current use of LUTSd medicine Overactive bladder Prostate No medicine c Use of LUTS aids Pads Catheter None d a DAN-PSS-1 questionnaire Symptom score Bother score Total score a Physical activity Walking distance, m Sports/exercise, minutes per week a Mobility velocity, Visual Analogue Scale (0–100mm) 39 Use of walking aids Crutch Rollator Other walking aids None Timed Up & Go test,40 no. per minute a One leg stand, eyes open, seconds Dominant leg Non-dominant leg b Previous PFMT Yes No
Control Group
n515 No. (%)
n515 No. (%)
P value
29 (29–30) 100 (100–100) 65 (50–87)
29 (28–30) 100 (100–100) 55 (50–63)
0.22 0.78 0.60
12 (80) 3 (20)
11 (73) 4 (27)
13 (87) 0 (0) 0 (0) 1 (7) 1 (7)
10 (67) 2 (13,3) 0 (0) 0 (0) 1 (7)
4 (27) 6 (40) 2 (13) 2 (13) 1 (7)
6 (40) 7 (47) 0 (0) 2 (13) 0 (0)
12 (80) 2 (13) 1 (7)
11 (73) 4 (27) 0 (0)
0.51
2 (13) 1 (7) 12 (80)
4 ((27) 1 (7) 10 (67)
0.74 ... 0.78
2 (13) 0 (0) 13 (87)
2 (13) 0 (0) 13 (87)
1.00 1.00
9 (7–11) 7 (4–9) 11 (7–14)
10 (6–13) 11 (6–13) 17 (18–24)
0.51 0.12 0.25
2000 (1000–5000) 0 (0–0) 53 (43–73)
0.78
0.74
0.68
2000 (1000–4000) 45 (0–120) 53 (46–77)
0.68 0.81 0.84
0 (0) 0 (0) 0 (0) 15 (100) 25 (11)
0 (0) 1 (7) 0 (0) 14 (93) 21 (10)
1.00
10 (5–29) 29 (4–30)
3 (11–15) 10 (1–30)
0.56 0.12
0 (0) 15 (100)
2 (13) 13 (87)
0.54
0.78
Note: UE: Lower extremities.. a Median (interquartile range). PFMT: pelvic floor muscle training. c LUTS: lower urinary tract symptoms. d DAN-PSS-1: the Danish Prostate Symptom Score. b
Additional question The results of the ED-induced bother (A1) showed in TG a tendency to a significant improvement from pre-test to post-test (P50.05), but no such improvement was shown for the CG (Table 4). There were
no significant differences between TG and CG either at post-test or follow-up (Table 4). The results of question A2 showed a higher rate in TG without the influence of ED medicine, aids or appliances compared to CG (TG: pre-test: 83%; post-test: 92%, Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
189
Tibaek et al.
The effect of PFMT in stroke
Table 4 Results of pelvic floor muscle training within and between groups reassured on erectile function in men with stroke IIEF-5
Treatment Group
Control Group
P value3
18 (5–24) 20 (5–25) 15 (5–25) 0.04* 0.80
16 (5–24) 18 (5–25) 11 (5–18) 0.32 0.18
0.97 0.84 0.08
2 (1–4) 4 (3–4) 3 (2–4) 0.05 0.70
4 (1–5) 3 (2–5) 3 (2–5) 0.32 0.32
0.62 0.69 0.88
a
IIEF-5 Pre-test (20/30) Post-test (21/30) Follow-up (19/30) P value1 P value2 a Bother question (A1) Pre-test Post-test Follow-up P value1 P value2
Note: P value1: the level of significance within pre-test and post-test of the two groups. P value2: the level of significance within pre-test and follow-up of the two groups. P value3: the level of significance between the two groups. a Median (interquartile range).
follow-up: 85% versus CG: pre-test: 63%; post-rest: 64%, follow-up: 63%), although no significant differences within (P50.32; P51.0; P50.32) or between groups (P50.81; P50.69; P50.33) were demonstrated.
Adverse events No participants in the TG and the CG reported any form of adverse event during the trial.
Discussion The results of this RCT showed that PFMT was associated with a better erectile function in men with LUTS after stroke, although the statistical precision was low. In addition, PFMT appeared well tolerated, with low drop-out rate, high session attendance, and no reported adverse events.
Figure 1 Results of International Index of Erectile Function (IIEF-5) questionnaire sum score presented as box plots.
190
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
Tibaek et al.
To our knowledge, the present study is the first RCT evaluating the effect of PFMT measured on erectile function in men with LUTS after stroke. van Kampen et al. evaluated the effect of a PFMT program in men with ED caused by different etiologies and they concluded that it might be a non-invasive alternative for the patients with ED caused by venous occlusion. However, the study did not have a control group and men with neurological diseases were excluded.19 Similarly, Dorey et al. evaluated the effect of a PFMT program in neurologically healthy men with ED and compared their findings with a control group. Their results showed, like ours, a significant improvement due to the intervention.32 In the present study, the results show that the median value of IIEF-5 sum score tends to decrease most at follow-up in the CG, indicating that PFMT may provide a long-term effect compared to no training. Moreover, the participants with less severe ED showed short-term effect at post-test in TG (Fig. 1) compared to none in the participants with less severe ED in CG. In addition, the target group with less severe ED did not change from post-test to follow-up in TG compared to markedly decrease in CG. This indicates that participants with less severe ED in the TG maintained their erectile function due to the PFMT compared to those in the CG who did not maintain their level of erectile function either in short-term or particularly in long-term (Fig. 1). The participants might still have some spontaneously remission due to the short time since last stroke; however, there were no significant difference between TG and CG.G in days since last stroke. Likewise, the participants in CG had more previous stroke (Table 2) than TG but without statistical significant difference. However, although a two-point change on IIEF-5 in TG versus CG did not present any clinical meaningful information in the present study; maybe it result in a psychosocial factor as motivation to improve sexual health. Moreover, at baseline, the participants reported mild ED. Had moderate-to-severe ED been reported in the participants, a potentially larger effect might be demonstrated. The mechanisms underlying the effect of PFMT on ED in men with stroke are not known. According to Goto et al. and Kratzik et al. moderate-intensity physical exercise leads to an increase in nitric oxide (NO) production, thus predicting endotheliumdependent vasodilatation.16,33 It seems possible that this effect may further improve erectile function, and that physical activity not only increase arterial
The effect of PFMT in stroke
blood supply to the penis but also increases the bioavailability of NO.6,16 However, the TG participants in this study did not perform sport/exercise above average level (cycling 15minute, running 15minute per week) at least at their baseline registration (Table 3). The fact that stroke is a vascular damage in the brain, the hypothesis with increased oxygen to the brain and the pelvic floor muscles due to the physical activity may be a protecting factor for development of ED has been explained by improved oxygen in the organs. This may be an interesting topic for further research. Another hypothesis of mechanisms underlying the effect of PFMT on ED may be the increased activity in ischiocavernosus and bulbocavernosus muscles leading to a higher pressure at the base of the penis according to the thesis for PFMT effect in neurologic healthy men with ED.19,20 The participants in the present study reported mild to moderate degree of LUTS at baseline and in a later publication we will report the effect of PFMT measured on DAN-PSS-1 questionnaire.27 In the present study, six (20%) participants reported that they were not sexually active, which is in line with results among 924 healthy Swedish men with a similar mean age of 65.30 Nine (30%) participants in our sample were ‘‘not married/partnered,’’ which may be one explanation for their sexual inactivity. Surprisingly few participants reported themselves as ‘‘dissatisfied’’ in relation to their ED-induced bother question (A1), which may be explained by their level of ED severity or by the fact that this is a group of men for whom erectile function is less relevant. Another explanation may be that sexualityrelated questions are too sensitive and private for the participants to communicate to a third party.
Methodological considerations Some methodological issues in this study need to be considered. The first is the small sample size notwithstanding the large number of screened medical records of men with stroke. The power calculation estimated a necessary sample size of 120 participants, but, due to the restrictive inclusion criteria, the number of included patients was much lower. This decrease in the statistical precision is a major limitation. In recent years, it has been difficult to include in research stroke patients at this phase of their rehabilitation regarding contemporary ongoing rehabilitations or medical examinations processes.23 Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
191
Tibaek et al.
The effect of PFMT in stroke
Secondly, the large amount of missing outcome data in the CG, reduces the internal validity of the study due to potential selection bias (informative missing). Collecting outcome data by self-administered sexuality-related questionnaires seem to be problematic in men.34 However, we could have used other methods to gather those missing answers such as a combination of qualitative and quantitative data. Qualitative methods, as focus groups, in-depth interviews, allow for a deeper understanding of the reasons why participants answer or not. Another method could be suggested for some participants who perhaps did not understand the questions (no information of education level) we could have asked the participants to complete the questionnaire with assistance of a nurse with experiences in sexual dysfunction35 In future, design using triangulation data by using a mix of methods and tools may give us insight to the processes leading to the outcomes. Thirdly, we defined the results at 6-month followup as a long-term effect. In previous RCTs, the interval between post-test and follow-up test varies between 1month and 10–15years depending on the severity and diagnosis in the study group. Fourthly, the pre-test of IIEF-5 was altered from 3months to 1-monthwhich weakened the validity of IIEF-5 questionnaire. Finally, the role of placebo effect present in this study. If we had used a RCT with blind assessor the influences of placebo effect was reduced. However, in trials as well as in clinical practices, evaluation of ED is a subjectively measure.
Perspectives Medical professionals in stroke rehabilitation need to improve their attitude and understanding of issues such as sexuality36 because sexual dysfunction after stroke also occurs in women.37 Therefore, knowledge from this first RCT evaluating the effect of PFMT measured on ED in men with LUTS after stroke may provide valuable information for research in the future.
Conclusions The results showed that PFMT measured on erectile function in men with LUTS after stroke may have short-term and long-term effects, although no significant effect was demonstrated within groups at longterm effect and between the groups for short-term and long-term effect. An evaluation is suggested into the effect of PFMT programs addressed through larger RCT in the rehabilitation of men with ED and LUTS after stroke. 192
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
Acknowledgements The authors wish to thank all the patients for participation. Big thanks are also due to Anette Lia, Department of Neurology, Glostrup Hospital and Sille Malene G Christensen, Department of Neurology, Herlev Hospital for their secretarial assistance. Thanks to all the staff at the Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen.
Disclaimer Statements Contributors S. Tibæk: Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting the manuscript, Revising It for intellectual content, Final Approval of the completed manuscript. G. Gard: Conception and design, drafting the manuscript, revising it for intellectual content, final approval of the completed manuscript. C. Dehlendorff: Conception and design, acquisition of data, analysis and interpretation of data, revising it for intellectual content, final approval of the completed manuscript. H.K. Iversen: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript. J. Erdal: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript. F. BieringSørensen: Conception and design, revising it for intellectual content, final approval of the completed manuscript. G. Dorey: Conception and design,revising it for intellectual content, final approval of the completed manuscript. R Jensen: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript.
Funding This study was supported by grants from the Association of Danish Physiotherapists Research Foundation, the Association of Danish Physiotherapists Practise Foundation, the Foundation of 17.12.1981, Lykkefeldts Grant, the Foundation of Lundbeck (UCSF) and the Department of Physiotherapy and Occupational Therapy Glostrup Hospital, University of Copenhagen.
Conflicts of interest The authors report no conflicts of interest.
Ethics approval The study was approved by the Ethical Committee of Copenhagen Capital Registration (H-B-2009-069) and registered in the Danish Register for Data protection.
Tibaek et al.
References 1 Bener A, Al-Hamaq AO, Kamran S, Al-Ansari A. Prevalence of erectile dysfunction in male stroke patients, and associated co-morbidities and risk factors. Int Urol Nephrol. 2008;40(3): 701–708. 2 Monga TN, Lawson JS, Inglis J. Sexual dysfunction in stroke patients. Arch Phys Med Rehabil. 1986;67(1):19–22. 3 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. Neurourol Urodyn. 2008;27:763–771. 4 Rees PM, Fowler CJ, Maas CP. Sexual function in men and women with neurological disorders. Lancet. 2007;369(9560): 512–525. 5 Berner MM, Leiber C, Kriston L, Stodden V, Gunzler C. Effects of written information material on help-seeking behavior in patients with erectile dysfunction: a longitudinal study. J Sex Med. 2008;5(2):436–447. 6 Cheng JY, Ng EM, Ko JS, Chen RY. Physical activity and erectile dysfunction: meta-analysis of population-based studies. Int J Impot Res. 2007;19(3):245–252. 7 Korpelainen JT, Nieminen P, Myllyla VV. Sexual functioning among stroke patients and their spouses. Stroke. 1999;30(4): 715–719. 8 Lue TF. Erectile dysfunction. N Engl J Med. 2000;342(24): 1802–1813. 9 Calabro RS, Gervasi G, Bramanti P. Male sexual disorders following stroke: an overview. Int J Neurosci. 2011;121(11): 598–604. 10 Tsao CW, Cha TL, Lee SS, et al. Association between lower urinary tract symptoms and sexual dysfunction in Taiwanese men. Andrologia. 2008;40(6):387–391. 11 Fazio L, Brock G. Erectile dysfunction: management update. CMAJ. 2004;170(9):1429–1437. 12 Goldstein I, Lue TF, Padma-Nathan H, Rosen RC, Steers WD, Wicker PA. Oral sildenafil in the treatment of erectile dysfunction. Sildenafil Study Group. N Engl J Med. 1998;338(20): 1397–1404. 13 Jung JH, Kam SC, Choi SM, Jae SU, Lee SH, Hyun JS. Sexual dysfunction in male stroke patients: correlation between brain lesions and sexual function. Urology. 2008;71(1):99–103. 14 Bacon CG, Mittleman MA, Kawachi I, Giovannucci E, Glasser DB, Rimm EB. A prospective study of risk factors for erectile dysfunction. J Urol. 2006;176(1):217–221. 15 Ponholzer A, Temml C, Obermayr R, Wehrberger C, Madersbacher S. Is erectile dysfunction an indicator for increased risk of coronary heart disease and stroke? Eur Urol. 2005;48(3): 517–518. 16 Kratzik CW, Lackner JE, Mark I, et al. How much physical activity is needed to maintain erectile function? Results of the Androx Vienna Municipality Study. Eur Urol. 2009;55(2):509–516. 17 Patel MI, Yao J, Hirschhorn AD, Mungovan SF. Preoperative pelvic floor physiotherapy improves continence after radical retropubic prostatectomy. Int J Urol. 2013;20(10):986–992. 18 Campbell SE, Glazener CM, Hunter KF, Cody JD, Moore KN. Conservative management for postprostatectomy urinary incontinence. Cochrane Database Syst Rev. 2012; (1):CD001843. 19 van Kampen M, de Weerdt W, Claes H, Feys H, de Maeyer M, van Poppel H. Treatment of erectile dysfunction by perineal exercise, electromyographic biofeedback, and electrical stimulation. Phys Ther. 2003;83(6):536–543. 20 Dorey G. Pelvic Floor Exercises for Erectile Dysfunction. 1st ed. London: Whurr Publishers; 2004; p. 78–79. 21 Dorey G, Speakman MJ, Feneley RC, Swinkels A, Dunn CD. Pelvic floor exercises for erectile dysfunction. BJU Int. 2005; 96(4):595–597. 22 Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Pena BM. Development and evaluation of an abridged, 5-item version
23 24 25 26
27
28
29
30
31 32
33
34
35 36
37 38 39
40
The effect of PFMT in stroke
of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res. 1999; 11(6):319–326. Tibaek S, Gard G, Jensen R. Pelvic floor muscle training is effective in women with urinary incontinence after stroke. Neurourol Urodyn. 2005;24(4):348–357. WHO WHO. WHO Task Force on Stroke and other cerebrovascular Disorders. Stroke-1989: recommendation on stroke prevention, diagnosis and therapy. Stroke. 1989;20:1407–1431. Folstein MF, Folstein SE, McHugh PR. ‘‘Mini-Mental State’’: a practical method for grading the cognitive state of the patients for the clinicians. Psychol Med. 1976;6:551–553. Abrams P, Cardozo L, Fall M, et al. The standardisation of terminology of lower urinary tract function: report from the Standardisation Sub-committee of the International Continence Society. Neurourol Urodyn. 2002;21:167–178. Meyhoff HH, Hald T, Nordling J, Andersen JA, Bilde T, Walter S. A new patient weighted symptom score (DAN-PSS-1). Clinical assessment of indications and outcomes of Transurethral prostatectomy for uncomplicated benign prostatic hyperplasia. Scand J Urol Nephrol. 1993;27:493–499. Nygaard IE, Kreder KJ, Lepic MM, Fountain KA, Romberg AT. Efficacy of pelvic floor muscle exercises in women with stress, urge, and mixed urinary incontinence. Am J Obstet Gynecol. 1996;174(1 Ot 1):120–125. Bø K, Hagen R, 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. Neurourol Urodyn. 1990;9(5):489–502. Stroberg P, Boman H, Gellerstedt M, Hedelin H. Relationships between lower urinary tract symptoms, the bother they induce and erectile dysfunction. Scand J Urol Nephrol. 2006;40(4): 307–312. R Development Core Team. A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2006. Dorey G, Speakman M, Feneley R, Swinkels A, Dunn C, Ewings P. Randomised controlled trial of pelvic floor muscle exercises and manometric biofeedback for erectile dysfunction. Br J Gen Pract. 2004;54(508):819–825. Goto C, Nishioka K, Umemura T, et al. Acute moderateintensity exercise induces vasodilation through an increase in nitric oxide bioavailiability in humans. Am J Hypertens. 2007; 20(8):825–830. Matthew AG, Currie KL, Irvine J, et al. Serial personal digital assistant data capture of health-related quality of life: a randomized controlled trial in a prostate cancer clinic. Health Qual Life Outcomes. 2007;5:38. Ozturk MI, Koca O, Keles MO, Gunes M, Kaya C, Karaman MI. Question for a questionnaire: the International Index of Erectile Function. Int J Impot Res. 2011;23(1):24–26. Soundy A, Stubbs B, Jenkins S, Cooper I. Sexual professional boundaries perceived by undergraduate and graduate physiotherapists: a cross sectional survey. Physiotherapy. 2013; 99(4):298–304. Tamam Y, Tamam L, Akil E, Yasan A, Tamam B. Post-stroke sexual functioning in first stroke patients. Eur J Neurol. 2008; 15(7):660–666. Mahoney FI, Barthel DW. Functional evaluation: The Barthel Index. Md State Med J. 1965;14:61–65. Tibaek S, Gard G, Klarskov P, Iversen HK, Dehlendorff C, Jensen R. Are activity limitations associated with lower urinary tract symptoms in stroke patients? A crosssectional, clinical survey. Scand J Urol Nephrol. 2009; 43(5):383–389. Podsiadlo D, Richardson S. The timed ‘‘Up & Go’’: a test of basic functional mobility for frail elderly persons. J Am Geriatr. Soc. 1991;39(2):142–148.
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
193
ISSN: 1074-9357 (Print) 1945-5119 (Online) Journal homepage: http://www.tandfonline.com/loi/ytsr20
The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke S. Tibaek, G. Gard, C. Dehlendorff, H. K. Iversen, J. Erdal, F. Biering-Sørensen, G. Dorey & R. Jensen To cite this article: S. Tibaek, G. Gard, C. Dehlendorff, H. K. Iversen, J. Erdal, F. BieringSørensen, G. Dorey & R. Jensen (2015) The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke, Topics in Stroke Rehabilitation, 22:3, 185-193, DOI: 10.1179/1074935714Z.0000000019 To link to this article: http://dx.doi.org/10.1179/1074935714Z.0000000019
Published online: 17 Mar 2015.
Submit your article to this journal
Article views: 59
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ytsr20 Download by: [University of Waterloo]
Date: 12 November 2016, At: 19:46
The effect of pelvic floor muscle training on sexual function in men with lower urinary tract symptoms after stroke S. Tibaek1, G. Gard2, C. Dehlendorff3, H. K. Iversen4, J. Erdal5, F. Biering-Sørensen6, G. Dorey7, R. Jensen4 1
Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen, Glostrup, Denmark, 2Department of Health Sciences, Division of Physiotherapy, Lund University, Lund, Sweden, 3 Danish Cancer Society Research Centre, Danish Cancer Society, Copenhagen, Denmark, 4Department of Neurology, Glostrup Hospital, University of Copenhagen, Denmark, 5Department of Neurology, Herlev Hospital, University of Copenhagen, Herlev, Denmark, 6Department of Spinal Cord Injuries, Glostrup Hospital, University of Copenhagen, Glostrup, Denmark, 7Department of Health and Applied Sciences, University of the West of England, Bristol, UK Background: Erectile dysfunction and lower urinary tract symptoms (LUTS) are common sequelae in men after stroke. Objective: The objective of this study was to evaluate the effect of pelvic floor muscle training (PFMT) on measured erectile function as an indicator of sexuality in men with LUTS after stroke. Method: A sample of 516 men with stroke was invited to participate in this single-blinded, randomized controlled trial according to in- and exclusion criteria. This resulted in 31 participants who were randomized to either a Treatment Group (n516) or a Control Group (n515). The intervention included 12weeks of PFMT. The effect was measured on the International Index of Erectile Function (IIEF-5) questionnaire. Results: Thirty participants (median age: 68 years; interquartile range: 60–74 years) completed the study, 15 in each group. The results of the IIEF-5 sum score showed a significant improvement (Pv0.04) from pre-test to post-test in the Treatment Group, but not in the Control Group. Within pre-test and 6-month follow-up, the median sum score decreased in both groups, worsened in the Control Group [Treatment Group, 3 (17%) versus Control Group, 5 (31%)]. There were differences between the groups at post-test and at follow-up, but they were not statistically significant. Conclusion: The results showed that, as measured by erectile function in men with LUTS after stroke, PFMT may have short-term and long-term effect, although no statistically significant effect was demonstrated between the groups. Keywords: Erectile function, LUTS, Men, Pelvic floor muscle training, Stroke
Introduction Erectile dysfunction (ED) is highly prevalent in men after stroke, ranging from 48 to 62%.1,2 However, it is seldom a consequence of stroke alone; physical and cognitive deficits, depression and lower urinary tract symptoms (LUTS)3 are likely to contribute. ED as an aspect of sexuality is an integral and important part of quality of life in men with stroke4–6 as it is for their partners.7 Particularly for stroke patients with LUTS, urinary incontinence during sexual activity can be challenging.
Correspondence to: S. Tibaek, Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen, Ndr. Ringvej 57, 2600, Glostrup, Denmark. Email: [email protected] ß W. S. Maney & Son Ltd 2015
DOI 10.1179/1074935714Z.0000000019
ED is defined as the consistent or recurrent inability of a man to obtain and/or maintain a penile erection sufficient for sexual performance.8 Erection requires intact vascular and neural functions and ED is linked to aging and a variety of co-existing medical conditions (hypertension, diabetes, cardiovascular disease, and LUTS).9,10 In addition, many of the antihypertensive agents commonly used by stroke patients may impair erection due to a concomitant lowering of the cavernosal arterial pressure; some (such as beta blockers) may also reduce sexual desire.4 The erectile blood flow, controlled by the autonomic erection centers, provides parasympathetic (S2–S4) and sympathetic (T12–L2) innervations to the pelvic plexus, which include the cavernous nerve Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
185
Tibaek et al.
The effect of PFMT in stroke
that innervate the cavernosal arteries and trabecular smooth muscle. The somatic motor nerve supply arises from the sacral spinal cord and innervates through the pudendal nerve the bulbocavernosus and ischiocavernosus muscles, which are active during ejaculation and climax.11 Treatment of ED in neurologically healthy men usually consists of pharmacotherapy,11,12 whereas there is little information on ED treatment in stroke patients.9,13 Physical activity has been shown to reduce the risk of ED14,15 and as measured by improvement in erection function score,6 may even reverse its development. Moreover, Kratzik et al. showed that physical exercise had a positive impact on men with ED.16 Pelvic floor muscle training (PFMT) has been shown to be effective on prostate pre- and postsurgical LUTS.17,18 Moreover, it was also found to have a significant effect in otherwise healthy men with ED19–21 measured by the International Index of Erectile Function (IIEF).22 Previously, PFMT has been shown to have a significant effect on urinary incontinence in women after stroke.23 Although ED and LUTS are highly prevalent in men with stroke and PFMT is effective in neurologically healthy men with ED and LUTS, we were not able to find published research data on the effect of PFMT in male stroke patients with ED and LUTS. The purpose of this study was to evaluate the effect of PFMT measured on erectile function as an indicator of sexuality in men with LUTS after stroke.
Methods This study is part of a large, multifaceted study focusing on PFMT in men with LUTS after stroke.
Participants Between 1 February 2010 and 31 December 2012, medical records of men with stroke from the Departments of Neurology, Glostrup and Herlev Hospitals, University of Copenhagen were successively screened by the project leader (ST) for inclusion according to the following inclusion and exclusion criteria. Inclusion criteria: (1) men diagnosed with stroke clinically according to the World Health Organization definition24 and/or confirmed by computer tomography or magnetic resonance scan; (2) at least 1 month since last stroke; (3) normal cognitive function (minimal mental examination score w25);25 (4) LUTS according to the International Continence Society definition,26 with start or aggravation close in time to the stroke and measured by the Danish Prostatic Symptoms Score (DAN-PSS-1) Questionnaire;27 186
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
(5) ability to walk independently indoors for at least 100m with or without walking aids; (6) ability to visit toilet independently; and (7) age w18years. Exclusion criteria: (1) prior history of LUTS surgery, pelvic surgery, or trauma; (2) more than two diagnosed strokes; (3) other severe neurological disease including dementia; (4) severe dysphasia; (5) severe psychiatric disease; (6) prostate cancer; and (7) inability to speak Danish or English. Demographic, neurological, urological, and physical baseline characteristics were obtained from the medical records and at the first study consultation.
Design The design was a prospective randomized, controlled and single-blinded, parallel group trial (RCT). A 4-week run-in period including an initial investigation sequence (pre-test) was followed by randomization to either a Treatment Group (TG) or a Control Group (CG). After 12weeks, the second investigation sequence was performed (post-test), with the final investigation sequence (follow-up) after further 6 months. Randomization was based on a mathematical table, delivered in blocks of 10 in sealed envelopes and managed by a person who did not participate further in the study. Registration of variables from the pre-test, posttest, and follow-up investigations sequences were managed by individuals (physiotherapists) who were blinded to the randomization code of the participants, while the physiotherapist treating the participants with PFMT was unblinded. The participants randomized for CG were all offered a 12-week PFMT program after the trial. The participants received verbal and written information and signed an informed consent before study entry. The study was approved by the Ethical Committee of Copenhagen Capital Registration (H-B-2009-069) and registered in the Danish Register for Data protection and in Clinical Trials.gov Protocol Registration System (Clinical Trials NTC01042249).
Intervention All the same, specialized physiotherapist, in a systematic, controlled, intensive PFMT program over 12 consecutive weeks, treated the participants in the TG. The procedure is presented in Table 1. The content of the treatment program: 1. Introduction (theory): information about prevalence and definition of LUTS, anatomy and physiology of the bladder and the pelvic floor muscle (PFM), motivation and instruction in home exercises. 2. Home exercises: PFM strengthening exercise by performing close to maximum contraction (6-second contraction/6-second rest);28 endurance
Tibaek et al.
Table 1 Pelvic floor muscle training program for men with stroke Introduction (theory)
60minutes
Group treatment Frequency
3–6 participants/group 1 session (60minutes) per week 12weeks i8 sessions
Duration Attendance in group -treatment sessions Digital anal palpation Home exercises
2–3 times 1–2 times daily
PFM exercise by performing sub-maximal contraction for as long as possible (max 30-second contraction/30-second rest). Participants were instructed to repeat the exercise program gradually 6–10 times in supine, standing and sitting positions, once or twice daily. 3. Group treatments consist of isolated PFM contraction (6-second contraction/6-second rest); strength exercises (3-second contraction/3-second rest, and 6-second contraction/6-second rest); endurance exercises (max 30-second sub-maximal contraction/ 30-second rest). Sub-maximal PFM contractions before and during coughing, sneezing, laughing, and in daily activities such as rising, sitting, and lifting. 4. All techniques were repeated 4–8 times in supine, standing and sitting positions, and during activates such as: slow and fast walking. 5. Digital anal palpation of PFM was performed to control correct contraction, to give continual feedback to the participants, and to evaluate the PFM strength. The participants in TG received only feedback at digital anal palpation 2–3 times.
The training program was a modified version of a standard program for group treatment of stress incontinence.23,29 The participants in the CG followed the normal, standard program of general rehabilitation without specific treatment for LUTS.
Main outcome measures The effect of PFMT was measured on the IIEF-5 questionnaire.22 The IIEF-5 assesses the prevalence and severity of ED according to the classification system developed by Rosen et al.22 It consists of five questions each scored from 0 to 5. Question number 1 addresses confidence in the erectile function, questions 2–4 the actual erectile function capacity, and question number 5 intercourse satisfaction. The IIEF-5 sum score is the sum of the ordinal responses to the five questions. The severity levels are classified for the sum score 22–255no ED, for 17–215mild ED, for 12–165mild to moderate ED, for 8–115moderate ED, and for 1–75severe ED.22 The IIEF-5 is a patient-administered questionnaire.
The effect of PFMT in stroke
In this study, the participants were asked to fill in the IIEF-5 based on the previous month in contrast to 3months in the original version.
Additional question The questionnaire included the following EDinduced bother question A1 ‘‘If you were to spend the rest of your life with your ED problems as they are now, how would you feel about that?’’ The answer was rated on an ordinal scale (1–5) (15very dissatisfied, 25some dissatisfaction, 35neither satisfied nor dissatisfied, 45some satisfaction, 55very satisfied).30 Followed by A2: ‘‘If you use medicine or other aids/appliances to optimize erection, is that reflected in your answer in question A1?’’ The answer was rated on a binominal scale (with, or without, medicine or aids/appliance).
Statistical analysis Statistical analyses were carried out using IBM SPSS (Statistical Package of Social Science) version 20. and R, version 2.5.0.31 Median and interquartile range are presented for small samples. The null-hypothesis between groups was tested by the Mann–Whitney U test and within groups using Wilcoxon signed rank test. For all tests, the level for statistical significant was set to Pv0.05. Power calculations showed that, with 90% power (beta50.9) and a significance level at P50.05, a total of 120 participants were needed for the study.
Results Participants Medical records of 1812 men with stroke were screened for inclusion and 516 were invited to participate in this RCT. Of these, 62 (12%) did not respond, 241 (47%) reported that they did not have any LUTS, while 113 (22%) had LUTS before the stroke and its status was unchanged, 13 (2%) had LUTS related to a history of prostate surgery but not noted in their medical records, 51 (10%) had LUTS, but no resources to participate or did not want to do so, leaving 36 (7%) for inclusion. However, five of these men did not show up for inclusion and pre-test (n51: ‘‘too much hospital’’; n54: no information), leaving 31 for inclusion. After the first investigation, sequence one participant (randomized to the TG) dropped out (unknown reason) before starting the PFMT sessions. The remaining 30 participants, 15 in each group, with a median age of 68 (interquartile range 60–74), completed the study. At follow-up, one participant from the CG was lost for follow-up. The trial had to be closed after 35months due to poor recruitment of participants. Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
187
Tibaek et al.
The effect of PFMT in stroke
Median PFMT session attendance rate in TG was 11 (interquartile range: 10–12), corresponding to 92%.
Characteristics Demographic baseline characteristics of the study group are presented in Table 2. Neurological, urological, and physical baseline characteristics are presented in Table 3. There were no significant differences between the TG and the CG for any baseline characteristics.
IIEF-5 The median IIEF-5 sum score at baseline was 17 (interquartile range: 5–23). The results (Table 4) showed a significant improvement in the TG from pre-test to post-test, but not in the CG. There were no statistical significant differences between TG and CG either at pre-test or at post-test (Fig. 1).
At 6-month follow-up, the results showed no significant difference between groups or within groups (pre-test versus follow-up). However, IIEF-5 sum scores within pre-test and follow-up were worsened in the CG (Table 4, Fig. 1). Data were missing in the TG (n52, 13%) and in the CG (n57–9, 47–60%). Six participants reported that they were not sexually active. Moreover, 3–5 participants failed to complete at least one out of five questions in the IIEF-5 questionnaire at pre-test, post-test, or follow-up, respectively, which made it impossible to calculate the IIEF-5 sum scores. The proportion of answering was as following: TG: pre-test587%; post-test587%; follow-up587% versus CG: pre-test547%; post-test564%; followup540%.
Table 2 Demographic baseline characteristics of men with stroke in the trial Treatment Group Characteristic Age, yearsa Past medical history, diseases and risk factors Stroke (one attack) Hypertension Transient ischemic attack Diabetes mellitus Coronary heart disease Other diseases (arthritis, fractures, muscular disorders, etc.) None Smoking Smoker Former smoker Never smoked No information Alcohol, no. consumed units per week 0 0–6 7–13 14–21 w21 No information Social status Employed Unemployed Early retired/sick leave w3months Retired No information Civil status Single/divorced Married/partnered Widower No information Current use of medication Antiarrhythnics/antihypertensives Statins Anticoagulants/antithrombotics Hypoglycaenics agents Analgesics Antidepressants Other No medicine Note: aMedian (interquartile range).
188
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
n515 No. (%) 68 (57–73) 0 4 0 2 3 5 7
(0) (27) (0) (13) (20) (33) (47)
2 (13) 3 (20) 10 (67) 0 (0) 5 5 2 2 1 0
(33) (33) (13) (13) (7) (0)
Control Group n515 No. (%) 70 (64–75) 5 5 1 1 0 5 2
P value 0.22
(33) (33) (7) (7) (0) (33) (13)
0.13 0.78 0.78 0.78 0.37 1.00 0.13
2 (13) 1 (7) 12 (80) 0 (0)
0.49
7 6 1 0 1 0
(47) (40) (7) (0) (7) (0)
0.33
5 (33) 0 (0) 1 (7) 9 (60) 0 (0)
2 (13) 0 (0) 3 (20) 10 (67) 0 (0)
0.57 -
4 (27) 10 (67) 1 (7) 0 (0)
4 (27) 11 (73) 0 (0) 0 (0)
0.84
10 (67%) 12 (80%) 12 (80%) 1 (7%) 1 (7%) 1 (7%) 5 (33%) 0 (0%)
6 (40%) 10 (67%) 12 (80%) 0 (0%) 1 (7%) 0 (0%) 7 (47%) 0 (0%)
0.22 0.54 1,00 0,77 1.00 0.77 0.54 1.00
Tibaek et al.
The effect of PFMT in stroke
Table 3 Neurological, urological, and physical baseline characteristics of men with stroke Treatment Group Characteristic Neurological a Mini-mental state examination score (maximum score530) a Barthel Index (maximum score5100) 38 a Time since last stroke, days Result of stroke verification by CT or MRI scan Visible stroke at imaging No visible stroke at imaging, but clinical stroke Subtypes of stroke Infarct Hemorrhage Infarctzhemorrhage No infarct No information Localisation Left hemisphere Right hemisphere Bilateral Unclassified No information Urological c Past history of LUTS None Pharmacological treatment No information Current use of LUTSd medicine Overactive bladder Prostate No medicine c Use of LUTS aids Pads Catheter None d a DAN-PSS-1 questionnaire Symptom score Bother score Total score a Physical activity Walking distance, m Sports/exercise, minutes per week a Mobility velocity, Visual Analogue Scale (0–100mm) 39 Use of walking aids Crutch Rollator Other walking aids None Timed Up & Go test,40 no. per minute a One leg stand, eyes open, seconds Dominant leg Non-dominant leg b Previous PFMT Yes No
Control Group
n515 No. (%)
n515 No. (%)
P value
29 (29–30) 100 (100–100) 65 (50–87)
29 (28–30) 100 (100–100) 55 (50–63)
0.22 0.78 0.60
12 (80) 3 (20)
11 (73) 4 (27)
13 (87) 0 (0) 0 (0) 1 (7) 1 (7)
10 (67) 2 (13,3) 0 (0) 0 (0) 1 (7)
4 (27) 6 (40) 2 (13) 2 (13) 1 (7)
6 (40) 7 (47) 0 (0) 2 (13) 0 (0)
12 (80) 2 (13) 1 (7)
11 (73) 4 (27) 0 (0)
0.51
2 (13) 1 (7) 12 (80)
4 ((27) 1 (7) 10 (67)
0.74 ... 0.78
2 (13) 0 (0) 13 (87)
2 (13) 0 (0) 13 (87)
1.00 1.00
9 (7–11) 7 (4–9) 11 (7–14)
10 (6–13) 11 (6–13) 17 (18–24)
0.51 0.12 0.25
2000 (1000–5000) 0 (0–0) 53 (43–73)
0.78
0.74
0.68
2000 (1000–4000) 45 (0–120) 53 (46–77)
0.68 0.81 0.84
0 (0) 0 (0) 0 (0) 15 (100) 25 (11)
0 (0) 1 (7) 0 (0) 14 (93) 21 (10)
1.00
10 (5–29) 29 (4–30)
3 (11–15) 10 (1–30)
0.56 0.12
0 (0) 15 (100)
2 (13) 13 (87)
0.54
0.78
Note: UE: Lower extremities.. a Median (interquartile range). PFMT: pelvic floor muscle training. c LUTS: lower urinary tract symptoms. d DAN-PSS-1: the Danish Prostate Symptom Score. b
Additional question The results of the ED-induced bother (A1) showed in TG a tendency to a significant improvement from pre-test to post-test (P50.05), but no such improvement was shown for the CG (Table 4). There were
no significant differences between TG and CG either at post-test or follow-up (Table 4). The results of question A2 showed a higher rate in TG without the influence of ED medicine, aids or appliances compared to CG (TG: pre-test: 83%; post-test: 92%, Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
189
Tibaek et al.
The effect of PFMT in stroke
Table 4 Results of pelvic floor muscle training within and between groups reassured on erectile function in men with stroke IIEF-5
Treatment Group
Control Group
P value3
18 (5–24) 20 (5–25) 15 (5–25) 0.04* 0.80
16 (5–24) 18 (5–25) 11 (5–18) 0.32 0.18
0.97 0.84 0.08
2 (1–4) 4 (3–4) 3 (2–4) 0.05 0.70
4 (1–5) 3 (2–5) 3 (2–5) 0.32 0.32
0.62 0.69 0.88
a
IIEF-5 Pre-test (20/30) Post-test (21/30) Follow-up (19/30) P value1 P value2 a Bother question (A1) Pre-test Post-test Follow-up P value1 P value2
Note: P value1: the level of significance within pre-test and post-test of the two groups. P value2: the level of significance within pre-test and follow-up of the two groups. P value3: the level of significance between the two groups. a Median (interquartile range).
follow-up: 85% versus CG: pre-test: 63%; post-rest: 64%, follow-up: 63%), although no significant differences within (P50.32; P51.0; P50.32) or between groups (P50.81; P50.69; P50.33) were demonstrated.
Adverse events No participants in the TG and the CG reported any form of adverse event during the trial.
Discussion The results of this RCT showed that PFMT was associated with a better erectile function in men with LUTS after stroke, although the statistical precision was low. In addition, PFMT appeared well tolerated, with low drop-out rate, high session attendance, and no reported adverse events.
Figure 1 Results of International Index of Erectile Function (IIEF-5) questionnaire sum score presented as box plots.
190
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
Tibaek et al.
To our knowledge, the present study is the first RCT evaluating the effect of PFMT measured on erectile function in men with LUTS after stroke. van Kampen et al. evaluated the effect of a PFMT program in men with ED caused by different etiologies and they concluded that it might be a non-invasive alternative for the patients with ED caused by venous occlusion. However, the study did not have a control group and men with neurological diseases were excluded.19 Similarly, Dorey et al. evaluated the effect of a PFMT program in neurologically healthy men with ED and compared their findings with a control group. Their results showed, like ours, a significant improvement due to the intervention.32 In the present study, the results show that the median value of IIEF-5 sum score tends to decrease most at follow-up in the CG, indicating that PFMT may provide a long-term effect compared to no training. Moreover, the participants with less severe ED showed short-term effect at post-test in TG (Fig. 1) compared to none in the participants with less severe ED in CG. In addition, the target group with less severe ED did not change from post-test to follow-up in TG compared to markedly decrease in CG. This indicates that participants with less severe ED in the TG maintained their erectile function due to the PFMT compared to those in the CG who did not maintain their level of erectile function either in short-term or particularly in long-term (Fig. 1). The participants might still have some spontaneously remission due to the short time since last stroke; however, there were no significant difference between TG and CG.G in days since last stroke. Likewise, the participants in CG had more previous stroke (Table 2) than TG but without statistical significant difference. However, although a two-point change on IIEF-5 in TG versus CG did not present any clinical meaningful information in the present study; maybe it result in a psychosocial factor as motivation to improve sexual health. Moreover, at baseline, the participants reported mild ED. Had moderate-to-severe ED been reported in the participants, a potentially larger effect might be demonstrated. The mechanisms underlying the effect of PFMT on ED in men with stroke are not known. According to Goto et al. and Kratzik et al. moderate-intensity physical exercise leads to an increase in nitric oxide (NO) production, thus predicting endotheliumdependent vasodilatation.16,33 It seems possible that this effect may further improve erectile function, and that physical activity not only increase arterial
The effect of PFMT in stroke
blood supply to the penis but also increases the bioavailability of NO.6,16 However, the TG participants in this study did not perform sport/exercise above average level (cycling 15minute, running 15minute per week) at least at their baseline registration (Table 3). The fact that stroke is a vascular damage in the brain, the hypothesis with increased oxygen to the brain and the pelvic floor muscles due to the physical activity may be a protecting factor for development of ED has been explained by improved oxygen in the organs. This may be an interesting topic for further research. Another hypothesis of mechanisms underlying the effect of PFMT on ED may be the increased activity in ischiocavernosus and bulbocavernosus muscles leading to a higher pressure at the base of the penis according to the thesis for PFMT effect in neurologic healthy men with ED.19,20 The participants in the present study reported mild to moderate degree of LUTS at baseline and in a later publication we will report the effect of PFMT measured on DAN-PSS-1 questionnaire.27 In the present study, six (20%) participants reported that they were not sexually active, which is in line with results among 924 healthy Swedish men with a similar mean age of 65.30 Nine (30%) participants in our sample were ‘‘not married/partnered,’’ which may be one explanation for their sexual inactivity. Surprisingly few participants reported themselves as ‘‘dissatisfied’’ in relation to their ED-induced bother question (A1), which may be explained by their level of ED severity or by the fact that this is a group of men for whom erectile function is less relevant. Another explanation may be that sexualityrelated questions are too sensitive and private for the participants to communicate to a third party.
Methodological considerations Some methodological issues in this study need to be considered. The first is the small sample size notwithstanding the large number of screened medical records of men with stroke. The power calculation estimated a necessary sample size of 120 participants, but, due to the restrictive inclusion criteria, the number of included patients was much lower. This decrease in the statistical precision is a major limitation. In recent years, it has been difficult to include in research stroke patients at this phase of their rehabilitation regarding contemporary ongoing rehabilitations or medical examinations processes.23 Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
191
Tibaek et al.
The effect of PFMT in stroke
Secondly, the large amount of missing outcome data in the CG, reduces the internal validity of the study due to potential selection bias (informative missing). Collecting outcome data by self-administered sexuality-related questionnaires seem to be problematic in men.34 However, we could have used other methods to gather those missing answers such as a combination of qualitative and quantitative data. Qualitative methods, as focus groups, in-depth interviews, allow for a deeper understanding of the reasons why participants answer or not. Another method could be suggested for some participants who perhaps did not understand the questions (no information of education level) we could have asked the participants to complete the questionnaire with assistance of a nurse with experiences in sexual dysfunction35 In future, design using triangulation data by using a mix of methods and tools may give us insight to the processes leading to the outcomes. Thirdly, we defined the results at 6-month followup as a long-term effect. In previous RCTs, the interval between post-test and follow-up test varies between 1month and 10–15years depending on the severity and diagnosis in the study group. Fourthly, the pre-test of IIEF-5 was altered from 3months to 1-monthwhich weakened the validity of IIEF-5 questionnaire. Finally, the role of placebo effect present in this study. If we had used a RCT with blind assessor the influences of placebo effect was reduced. However, in trials as well as in clinical practices, evaluation of ED is a subjectively measure.
Perspectives Medical professionals in stroke rehabilitation need to improve their attitude and understanding of issues such as sexuality36 because sexual dysfunction after stroke also occurs in women.37 Therefore, knowledge from this first RCT evaluating the effect of PFMT measured on ED in men with LUTS after stroke may provide valuable information for research in the future.
Conclusions The results showed that PFMT measured on erectile function in men with LUTS after stroke may have short-term and long-term effects, although no significant effect was demonstrated within groups at longterm effect and between the groups for short-term and long-term effect. An evaluation is suggested into the effect of PFMT programs addressed through larger RCT in the rehabilitation of men with ED and LUTS after stroke. 192
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
Acknowledgements The authors wish to thank all the patients for participation. Big thanks are also due to Anette Lia, Department of Neurology, Glostrup Hospital and Sille Malene G Christensen, Department of Neurology, Herlev Hospital for their secretarial assistance. Thanks to all the staff at the Department of Physiotherapy and Occupational Therapy, Glostrup Hospital, University of Copenhagen.
Disclaimer Statements Contributors S. Tibæk: Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting the manuscript, Revising It for intellectual content, Final Approval of the completed manuscript. G. Gard: Conception and design, drafting the manuscript, revising it for intellectual content, final approval of the completed manuscript. C. Dehlendorff: Conception and design, acquisition of data, analysis and interpretation of data, revising it for intellectual content, final approval of the completed manuscript. H.K. Iversen: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript. J. Erdal: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript. F. BieringSørensen: Conception and design, revising it for intellectual content, final approval of the completed manuscript. G. Dorey: Conception and design,revising it for intellectual content, final approval of the completed manuscript. R Jensen: Conception and design, acquisition of data, revising it for intellectual content, final approval of the completed manuscript.
Funding This study was supported by grants from the Association of Danish Physiotherapists Research Foundation, the Association of Danish Physiotherapists Practise Foundation, the Foundation of 17.12.1981, Lykkefeldts Grant, the Foundation of Lundbeck (UCSF) and the Department of Physiotherapy and Occupational Therapy Glostrup Hospital, University of Copenhagen.
Conflicts of interest The authors report no conflicts of interest.
Ethics approval The study was approved by the Ethical Committee of Copenhagen Capital Registration (H-B-2009-069) and registered in the Danish Register for Data protection.
Tibaek et al.
References 1 Bener A, Al-Hamaq AO, Kamran S, Al-Ansari A. Prevalence of erectile dysfunction in male stroke patients, and associated co-morbidities and risk factors. Int Urol Nephrol. 2008;40(3): 701–708. 2 Monga TN, Lawson JS, Inglis J. Sexual dysfunction in stroke patients. Arch Phys Med Rehabil. 1986;67(1):19–22. 3 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. Neurourol Urodyn. 2008;27:763–771. 4 Rees PM, Fowler CJ, Maas CP. Sexual function in men and women with neurological disorders. Lancet. 2007;369(9560): 512–525. 5 Berner MM, Leiber C, Kriston L, Stodden V, Gunzler C. Effects of written information material on help-seeking behavior in patients with erectile dysfunction: a longitudinal study. J Sex Med. 2008;5(2):436–447. 6 Cheng JY, Ng EM, Ko JS, Chen RY. Physical activity and erectile dysfunction: meta-analysis of population-based studies. Int J Impot Res. 2007;19(3):245–252. 7 Korpelainen JT, Nieminen P, Myllyla VV. Sexual functioning among stroke patients and their spouses. Stroke. 1999;30(4): 715–719. 8 Lue TF. Erectile dysfunction. N Engl J Med. 2000;342(24): 1802–1813. 9 Calabro RS, Gervasi G, Bramanti P. Male sexual disorders following stroke: an overview. Int J Neurosci. 2011;121(11): 598–604. 10 Tsao CW, Cha TL, Lee SS, et al. Association between lower urinary tract symptoms and sexual dysfunction in Taiwanese men. Andrologia. 2008;40(6):387–391. 11 Fazio L, Brock G. Erectile dysfunction: management update. CMAJ. 2004;170(9):1429–1437. 12 Goldstein I, Lue TF, Padma-Nathan H, Rosen RC, Steers WD, Wicker PA. Oral sildenafil in the treatment of erectile dysfunction. Sildenafil Study Group. N Engl J Med. 1998;338(20): 1397–1404. 13 Jung JH, Kam SC, Choi SM, Jae SU, Lee SH, Hyun JS. Sexual dysfunction in male stroke patients: correlation between brain lesions and sexual function. Urology. 2008;71(1):99–103. 14 Bacon CG, Mittleman MA, Kawachi I, Giovannucci E, Glasser DB, Rimm EB. A prospective study of risk factors for erectile dysfunction. J Urol. 2006;176(1):217–221. 15 Ponholzer A, Temml C, Obermayr R, Wehrberger C, Madersbacher S. Is erectile dysfunction an indicator for increased risk of coronary heart disease and stroke? Eur Urol. 2005;48(3): 517–518. 16 Kratzik CW, Lackner JE, Mark I, et al. How much physical activity is needed to maintain erectile function? Results of the Androx Vienna Municipality Study. Eur Urol. 2009;55(2):509–516. 17 Patel MI, Yao J, Hirschhorn AD, Mungovan SF. Preoperative pelvic floor physiotherapy improves continence after radical retropubic prostatectomy. Int J Urol. 2013;20(10):986–992. 18 Campbell SE, Glazener CM, Hunter KF, Cody JD, Moore KN. Conservative management for postprostatectomy urinary incontinence. Cochrane Database Syst Rev. 2012; (1):CD001843. 19 van Kampen M, de Weerdt W, Claes H, Feys H, de Maeyer M, van Poppel H. Treatment of erectile dysfunction by perineal exercise, electromyographic biofeedback, and electrical stimulation. Phys Ther. 2003;83(6):536–543. 20 Dorey G. Pelvic Floor Exercises for Erectile Dysfunction. 1st ed. London: Whurr Publishers; 2004; p. 78–79. 21 Dorey G, Speakman MJ, Feneley RC, Swinkels A, Dunn CD. Pelvic floor exercises for erectile dysfunction. BJU Int. 2005; 96(4):595–597. 22 Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Pena BM. Development and evaluation of an abridged, 5-item version
23 24 25 26
27
28
29
30
31 32
33
34
35 36
37 38 39
40
The effect of PFMT in stroke
of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res. 1999; 11(6):319–326. Tibaek S, Gard G, Jensen R. Pelvic floor muscle training is effective in women with urinary incontinence after stroke. Neurourol Urodyn. 2005;24(4):348–357. WHO WHO. WHO Task Force on Stroke and other cerebrovascular Disorders. Stroke-1989: recommendation on stroke prevention, diagnosis and therapy. Stroke. 1989;20:1407–1431. Folstein MF, Folstein SE, McHugh PR. ‘‘Mini-Mental State’’: a practical method for grading the cognitive state of the patients for the clinicians. Psychol Med. 1976;6:551–553. Abrams P, Cardozo L, Fall M, et al. The standardisation of terminology of lower urinary tract function: report from the Standardisation Sub-committee of the International Continence Society. Neurourol Urodyn. 2002;21:167–178. Meyhoff HH, Hald T, Nordling J, Andersen JA, Bilde T, Walter S. A new patient weighted symptom score (DAN-PSS-1). Clinical assessment of indications and outcomes of Transurethral prostatectomy for uncomplicated benign prostatic hyperplasia. Scand J Urol Nephrol. 1993;27:493–499. Nygaard IE, Kreder KJ, Lepic MM, Fountain KA, Romberg AT. Efficacy of pelvic floor muscle exercises in women with stress, urge, and mixed urinary incontinence. Am J Obstet Gynecol. 1996;174(1 Ot 1):120–125. Bø K, Hagen R, 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. Neurourol Urodyn. 1990;9(5):489–502. Stroberg P, Boman H, Gellerstedt M, Hedelin H. Relationships between lower urinary tract symptoms, the bother they induce and erectile dysfunction. Scand J Urol Nephrol. 2006;40(4): 307–312. R Development Core Team. A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2006. Dorey G, Speakman M, Feneley R, Swinkels A, Dunn C, Ewings P. Randomised controlled trial of pelvic floor muscle exercises and manometric biofeedback for erectile dysfunction. Br J Gen Pract. 2004;54(508):819–825. Goto C, Nishioka K, Umemura T, et al. Acute moderateintensity exercise induces vasodilation through an increase in nitric oxide bioavailiability in humans. Am J Hypertens. 2007; 20(8):825–830. Matthew AG, Currie KL, Irvine J, et al. Serial personal digital assistant data capture of health-related quality of life: a randomized controlled trial in a prostate cancer clinic. Health Qual Life Outcomes. 2007;5:38. Ozturk MI, Koca O, Keles MO, Gunes M, Kaya C, Karaman MI. Question for a questionnaire: the International Index of Erectile Function. Int J Impot Res. 2011;23(1):24–26. Soundy A, Stubbs B, Jenkins S, Cooper I. Sexual professional boundaries perceived by undergraduate and graduate physiotherapists: a cross sectional survey. Physiotherapy. 2013; 99(4):298–304. Tamam Y, Tamam L, Akil E, Yasan A, Tamam B. Post-stroke sexual functioning in first stroke patients. Eur J Neurol. 2008; 15(7):660–666. Mahoney FI, Barthel DW. Functional evaluation: The Barthel Index. Md State Med J. 1965;14:61–65. Tibaek S, Gard G, Klarskov P, Iversen HK, Dehlendorff C, Jensen R. Are activity limitations associated with lower urinary tract symptoms in stroke patients? A crosssectional, clinical survey. Scand J Urol Nephrol. 2009; 43(5):383–389. Podsiadlo D, Richardson S. The timed ‘‘Up & Go’’: a test of basic functional mobility for frail elderly persons. J Am Geriatr. Soc. 1991;39(2):142–148.
Topics in Stroke Rehabilitation
2015
VOL .
22
NO .
3
193
