J Neurol (2009) 256:1126–1133 DOI 10.1007/s00415-009-5083-9
ORIGINAL COMMUNICATION
Quality of life and neurobehavioral changes in survivors of malignant middle cerebral artery infarction Bessy Benejam Æ Juan Sahuquillo Æ Maria Antonia Poca Æ Laura Frascheri Æ Elisabeth Solana Æ Pilar Delgado Æ Carme Junque´
Received: 13 December 2008 / Revised: 15 February 2009 / Accepted: 18 February 2009 / Published online: 14 March 2009 Ó Springer-Verlag 2009
Abstract Malignant middle cerebral artery (MMCA) infarction is associated with a mortality rate of 80% under conservative treatment. Decompressive hemicraniectomy (DH) reduces mortality and improves the functional outcome of surviving patients. The purpose of this study was to examine quality of life (QoL) and neurobehavioral deficits in patients with space-occupying infarctions of the right- or left-sided hemisphere at 6 months after stroke. The Sickness Impact Profile (SIP) was used to assess QoL in 19 out of 29 consecutive patients that underwent DH after a malignant MCA infarction (14 on the right and 5 on B. Benejam J. Sahuquillo M. A. Poca E. Solana Neurosurgery and Neurotraumatology Research Unit, Vall d’Hebron University Hospital and Vall d’Hebron Research Institute, Universitat Auto`noma de Barcelona, Barcelona, Spain e-mail:
[email protected] J. Sahuquillo (&) M. A. Poca Department of Neurosurgery, Vall d’Hebron University Hospital and Vall d’Hebron Research Institute, Universitat Auto`noma de Barcelona, Passeig Vall d’Hebron 119-129, 08035 Barcelona, Spain e-mail:
[email protected] L. Frascheri Institute of Diagnostic Imaging, Vall d’Hebron University Hospital and Vall d’Hebron Research Institute, Universitat Auto`noma de Barcelona, Barcelona, Spain P. Delgado Department of Neurology, Vall d’Hebron University Hospital and Vall d’Hebron Research Institute, Universitat Auto`noma de Barcelona, Barcelona, Spain C. Junque´ Department of Psychiatry and Clinical Psychobiology, University of Barcelona, Barcelona, Spain
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the left hemisphere). Behavioral changes were evaluated with the Frontal Behavioral Inventory and the Beck Depression Inventory. Patients and relatives were also asked if, knowing the present outcome, they would agree again, in retrospect, to a DH. Barthel Index [60 was seen in 37% of our patients. Functional outcome was related to age. We found a higher reduction in the SIP’s physical domain than in the psychosocial domain. Depressive symptoms were present in 50% of the patients. We didn’t find significant differences in QoL or functional outcome between patients with right or left-sided infarctions. The most frequent neurobehavioral symptoms were decreased speech output, apathy, reduced spontaneity and irritability. Most patients and their relatives would again give consent to hemicraniectomy. The results show that younger patients had a significantly better outcome. QoL seems to be acceptable in both left- and right-sided infarctions, and retrospective agreement to hemicraniectomy is high in both patients and their relatives. Keywords Malignant middle cerebral artery infarction Quality of life Neurobehavioral outcome Decompressive hemicraniectomy Stroke
Introduction In patients with a malignant middle cerebral artery (MMCA) infarction treated conservatively, mortality can be as high as 80% [3, 13]. In the last few years, mortality has been partially improved through the use of moderate hypothermia [10] and dramatically reduced by decompressive hemicraniectomy (DH). The recent publication in Lancet Neurology of the pooled analysis of three european randomized clinical trials has provided level A evidence
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for recommending this procedure to reduce mortality in these patients [30]. This study demonstrated that DH reduces mortality to 17–25% and increases the number of patients with a favorable functional outcome [16, 30, 31]. However, despite this robust evidence, there are ongoing controversies on whether the trade-off of death for survival in a status of severe disability is worthwhile [21, 29]. As remarked by Puetz et al. [21], patient and family-centered measures of health-related quality of life (QoL) are necessary for a better understanding of the meaning of survival with severe disability and whether or not some type of severe disabilities could be considered a desirable outcome. Most previous studies on outcome after DH have focused on functional recovery. The most commonly used scales to measure outcome are the Barthel Index (BI) and the Modified Ranking Scale (mRS). A favorable outcome is generally defined as a BI [60 or an mRS B3 [26]. However, there is a need to use scales that measure the true impact of stroke, taking into account not only physical disability, but also the effect on social interaction, occupational or academic activities, communication skills and cognitive and emotional functions. An additional unsolved problem is whether patients with large brain infarctions in the dominant hemisphere should receive the same treatment as those with infarctions in the non-dominant hemisphere. Some centers exclude patients with left-sided infarctions because of the expectation of a very poor clinical outcome [5, 7, 22]. In contrast, other centers advocate the same treatment in all patients with MMCA infarctions, arguing that the true residual language deficits are still not very well known and that preliminary experience shows that language deficits are less severe than expected [17, 22, 23, 33]. The main goal of this study was to describe functional outcome, QoL and neurobehavioral changes in a cohort of patients who survived after DH for both dominant and nondominant MMCA infarction. A secondary aim was to determine whether these patients would agree to undergo decompressive craniectomy again, taking into account their current neurological outcome as well as the families’ satisfaction with the treatment.
Materials and methods Between March 2002 and February 2007, 29 patients with a MMCA infarction were treated in the NeuroICU of Vall d’Hebron University Hospital according to our institutional protocol, which combines induced moderate hypothermia (32–338C) with elective DH in patients presenting with a total anterior circulation syndrome, a neuroimaging study (MRI and/or CT scan) showing infarction of more than 50% of the MCA territory, with or without involvement of
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the basal ganglia, and an age below or equal to 65 years. In patients admitted within 24 h of stroke onset and with a CT scan showing a less than 5-mm midline shift, moderate hypothermia was induced by intravascular methods (Alsius Corporation, Irvine, CA). When patients had a midline shift C5 mm or intracranial hypertension (ICP [20 mmHg), decompressive surgery was indicated. Hypothermia was not induced in patients admitted after the first 24 h from stroke onset. Exclusion criteria for this treatment protocol were: (1) age [65 years, (2) patient or family refusal of treatment, (3) previous functional disability assessed by the mRS score (score [2) and (4) any condition that reduced life expectancy to less than 2 years (see Fig. 1 for therapeutic algorithm). Neurological status was evaluated upon admission to the intensive care unit (ICU) using both the Glasgow Coma Scale (GCS) and the National Institute of Health Stroke Scale (NIHSS). In the 20 survivors, functional outcome, QoL and neuropsychological deficits were evaluated by an independent research psychologist at 6 months after stroke. The study was approved by the local ethics committee (protocol PR-HG-128/2004). Informed consent was obtained from the patients or their legal representatives. Neuroradiological studies CT scans were performed at admission and at least once daily before decompressive craniectomy. All CT scans were done with a Phillips MX-8000, a 3-mm slice thickness, and a 512 9 512 matrix. The total volume of the hypodense brain in the CT scan was measured using a semi-automated method based on the ‘‘seeded region growing algorithm’’ expressed in cubic centimeters [8]. Instruments used to evaluate functional outcome and quality of life Functional outcome was assessed using the mRS [32] and dependency in activities of daily living by the Barthel Index (BI) [20]. With the BI, a score of less than 60 indicates that the individual is functionally dependent. QoL was assessed using the Spanish version of the Sickness Impact Profile (SIP) [1]. This instrument is a generic and robust measure of health status composed of 136 items grouped into 12 categories. The physical dimension is constituted by three categories: ambulation, mobility and body care. The psychosocial dimension is constituted by four additional categories: communication, emotional behavior, alertness behavior and social interaction. The remaining five categories are independent subscales: sleep and rest, eating, work, home management and recreation. Scores are presented as the percentage of
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Admission < 24 hours
Admission > 24 hours
GCS > 8
Heart disease
Intubation
Hemodynamic stability
Coagulopathy
NeuroICU
Normal pupils
Hematological abnormalities
Neuromonitoring
Midline shift < 5 mm
Important peripheric vascular disease
Medical Treatment
Intubation
Intubation
ICP > 20 mmHg
NeuroICU
NeuroICU
Midline shift ≥ 5 mm
Neuromonitoring
Neuromonitoring
Moderate Hypothermia
Medical Treatment
Medical Treatment
12 patients
17 patients
No written informed consent
ICP > 20 mmHg
Decompressive Hemicraniectomy
Midline shift ≥ 5 mm
29 patients
Fig. 1 Summary of the therapeutic algorithm applied in the treatment of malignant MCA infarction at our institution. A decompressive hemicraniectomy was performed on 29 patients. Moderate hypothermia
(32–338C) was induced before surgery in 12 of these 29 patients. Nine of these 29 patients died (6 from the hypothermia/decompressive treatment group and 3 from the decompressive surgery group)
maximal dysfunction and may range from 0 (no reduction in QoL) to 100 (maximal reduction in QoL).
disinhibition, poor judgement, social inappropriateness, impulsivity, hypersexuality, etc. The total score is obtained by adding the highest score reached for each of the 24 items. Each item is compared with the premorbid state and is scored 0 when no changes exist, 1 when changes are mild, 2 when moderate and 3 when severe. The maximum total score is 72. The threshold to diagnose a frontal syndrome is usually a cutoff score of 27, as suggested by Kertesz et al. [18].
Neuropsychological assessment The following instruments were used: (1) the Beck Depression Inventory (BDI) [2] to assess the presence and severity of depressive symptoms and (2) the Frontal Behavioral Inventory (FBI) [18] to describe and quantify behavioral and personality changes. The BDI is composed of 21 questions. Each question has a set of at least four possible choices ranging in intensity. The standard cutoffs are as follows: 0–9 (no depression), 10–18 (mild-moderate depression), 19–29 (moderate-severe depression) and 30– 63 (severe depression). Behavioral changes were assessed with the Frontal Behavioral Inventory (FBI). This test is a 24-item questionnaire administered to describe and quantify behavioral and personality changes in patients suffering from different forms of dementia. These items represent both negative and positive behaviors, such as apathy, spontaneity, emotional indifference, personal neglect, inattention, loss of insight,
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Retrospective agreement to decompressive hemicraniectomy Patients and caregivers were independently and privately asked to indicate, in retrospect and considering the actual outcome, whether they would again agree to DH treatment. The following three answers were recorded: ‘‘yes,’’ ‘‘no’’ and ‘‘I don’t know.’’ Statistical analysis All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS) version 12.0 for
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Table 1 Clinical and demographic data of the study group No
Age
Sex
GCS
NIHSS
Infarction
Side
Delay stroke-surgery (days)
Etiology
1
54
M
13
16
Partial MCA
Right
5
Thrombotic
2
65
M
14
21
Complete MCA, ACA
Left
3
Thrombotic
3
42
M
13
21
Complete MCA
Left
2
Thrombotic
4
65
M
14
21
Complete MCA
Right
2
Thrombotic
5
48
F
14
17
Partial MCA
Right
2
ICA dissection
6
55
M
15
18
Complete MCA
Right
4
Thrombotic
7 8
55 58
F M
8 12
– 18
Complete MCA Complete MCA
Right Right
1 1
Postsurgical Thrombotic
9
36
F
12
18
Partial MCA
Right
3
ICA dissection
10
61
M
15
17
Complete MCA
Right
6
Thrombotic
11
38
M
13
19
Complete MCA
Right
1
Thrombotic
12
44
M
13
21
Complete MCA, ACA
Left
1
Cardioembolic
13
53
M
14
20
Complete MCA
Right
1
MCA anerysm
14
61
M
10
21
Complete MCA
Left
3
Thrombotic
15
50
F
14
17
Partial MCA, ACA
Right
5
ICA dissection
16
51
M
14
19
Complete MCA
Right
3
Thrombotic
17
48
M
14
18
Partial MCA
Right
4
Thrombotic
18
19
F
7
20
Complete MCA, ACA
Left
2
Unknown
19
25
F
10
16
Complete MCA, ACA
Right
1
Postsurgical
MCA middle cerebral artery, ACA anterior cerebral artery, ICA internal carotid artery – unavailable data
Windows (distributed by SPSS Inc., Chicago, IL). Normally distributed variables were described by the mean and the standard deviation. The median and the range were used to describe variables that followed a non-normal distribution and ordinal variables, such as GCS, NIHSS, mRS, BI, SIP and BDI. The comparison of mean values was performed using the Student’s t test. The correlation between variables was calculated using Pearson’s correlation test. Cross-tabulations and the chi-square test were used to compare the frequency of occurrence of items among different outcome groups. Mann-Whitney U test was used to compare QoL subscales between right and leftsided infarctions. Differences were considered statistically significant when P B 0.05.
Results Twenty out of 29 operated patients (68.9%) survived after MMCA infarction. The nine deaths occurred within the first month after stroke. Three patients died from brain edema despite DH, one died due to medical complications (pneumonia), three patients experienced contralateral infarctions, one died due to pulmonary embolism and one due to cardiac arrest. The mean age of the nine patients who died was 56.1 ± 10.8 (median 59; range 32–68). Five of these patients had a dominant infarction and four a non-
dominant infarction. The median GCS and NIHSS scores upon admission to the ICU of these nine patients were 13.5 (range 10–15) and 19 (range 16–23), respectively. Before DH, mean midline shift was 8.8 ± 3.8, and the mean total volume of hypodense tissue in the CT scan was 267.2 ± 101.2 cc (median 278; range 144–423). The median time from stroke to surgery was 2 days (range 0– 3). Moderate hypothermia (32–338C) was induced before surgery in six of the nine patients (66.7%). Outcome assessment could not be performed in 1 of the 20 surviving patients because she left the country before the 6-month follow-up. The results of this study focused on the remaining 19 patients. These patients were assessed 6.47 ± 0.7 months after stroke. In Table 1 clinical and demographic data of the 19 patients are displayed. The mean age was 49.4 ± 12.6 years (median 51; range 20– 66). Before DH, the midline shift was 9 ± 3.2 mm, and the mean total volume of hypodense tissue in the CT scan was 236.2 ± 95.4 cc. Moderate hypothermia (32–338C) was induced before surgery in 10 of these 19 patients (52.6%). Functional outcome and QoL Using the traditional dichotomization of the mRS, five patients (26.3%) achieved a favorable outcome (defined as an mRS of 0–3). The remaining 14 patients (73.7%) had a mRS score of 4, indicating moderate severe disability
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Quality of life subscales
Range
Median
IQ 25–75
Total score
29–61
37
33–44
Physical score
20–69
41
36–51
Psychosocial score
7–61
29
18–30
Ambulation
26–57
41
33–50
Mobility
0–65
18
9–34
Body care and movement
21–82
52
45–57
(50%) had no signs of depression, eight had signs of mild depression, three were moderately depressed, and two were severely depressed. Mean FBI score was 18.2 ± 9.7 (median 15; range 7–37). The most frequent behavioral changes after MMCA infarction were an increase in impulsivity (87% of patients), logopenia (67%), lack of spontaneity (60%), apathy (60%), verbal apraxia (a speech disorder associated with a difficulty in initiating, coordinating or sequencing the muscle movements necessary to speak) (53%) and irritability (53%).
Communication Emotional behavior
0–72 0–75
11 22
0–41 10–41
Retrospective agreement with surgical treatment
Alertness behavior
0–100
29
19–46
Table 2 Subscales of the SIP in the 19 patients of the study group 6 months after decompressive craniectomy
Social interaction
10–64
23
18–31
Sleep and rest
10–73
31
22–33
Eating
8–86
12
12–19
Work
88
88
88–88
Home management
13–86
71
61–86
Recreation and pastimes
0–79
30
18–54
(patients unable to walk without assistance and unable to attend to own bodily needs without assistance). No patient had a mRS of 5 (severe disability). Patients with favorable outcome were significantly younger than patients with unfavorable outcome (mean 36.4 ± 14.3 and 54.1 ± 8.3 years, respectively; P = 0.004). Disability measured using the BI revealed a mean score of 51.3 ± 21.9 (median 45; range 10–95). In seven patients (37%), BI was at least 60, indicating a favorable outcome. Patients with a higher BI were significantly younger than patients with poor functional outcome. Mean age of patients with a BI C60 was 40.1 ± 13.3, while for patients with a BI \60, mean age was 54.8 ± 8.8 (P = 0.01). In our study the SIP was selected because in a review by Buck et al. it was one of the best generic measures to exhibit all the required psychometric properties of reliability, validity and responsiveness [4]. The mean total SIP score in survivors was 38.2 ± 8.4% (median 37; range 29– 61). The scores were higher in the physical (42.3 ± 12.9%; median 41; range 20–69) than in the psychosocial domain (26.6 ± 12.3%; median 29; range 7–61), indicating a more severe dysfunction in the former area. Table 2 summarizes the scores in each of the SIP categories. QoL was not related to functional outcome measured by the mRS, nor was it related to initial neurological status, the volume of the infarcted tissue or the time from stroke to surgery.
We found that 79% of surviving patients and 95% of caregivers retrospectively agreed that the decision to undergo DH was correct and would choose this option again. Retrospective agreement to surgery of the surviving patients was not related to the total volume of infarction, nor to the severity of functional outcome, nor to the extent of QoL reduction. Language deficits and outcome There were 5 patients with a left-dominant infarction and 14 with a non-dominant infarction. One of the patients with a left-sided infarction had a mixed transcortical aphasia and four had global aphasia, although two of them presented an incomplete aphasic syndrome. Both patients were able to match spoken words with their corresponding drawings and preserved some auditory–verbal comprehension for simple commands. The other two patients with global aphasia were extremely impaired in both comprehension and expression of language. No statistically significant differences in functional outcome evaluated by the BI and mRS were found between patients with dominant and non-dominant MMCA infarction (P = 0.40 and P = 0.43, respectively). When comparing QoL profiles, patients with right-sided stroke performed better in the communication subscale of the SIP (right-sided: median 8, range 0–41; left-sided: median 60, range 30–72; P = 0.001). However, there were no significant differences between both groups in the remaining QoL subscales (Fig. 2). Caregiver and patient agreement with the decision to undergo the same treatment was not related to the side of the infarction. In fact, all five patients with a left-sided infarction, as well as their relatives, would have made the same decision again.
Behavioral and personality changes Discussion BDI was performed in 16 of the 19 patients. In the remaining three patients, BDI could not be administered due to important language impairment. Eight patients
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As far as we know, this study is one of the few that evaluates not only physical disability and QoL, but also
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Fig. 2 Sickness Impact Profile scores for patients with rightand left-sided infarctions. Significant differences were found only in communication subscale, with higher scores in the left-sided stroke group
neurobehavioral changes and personal and family satisfaction after DH in patients with a MMCA infarction. In this study, despite substantial residual disability and the timing of evaluation being only 6 months after stroke, most patients and their families did not regret the decision to consent to DH. This was the case in all patients with large infarctions in the dominant hemisphere. Because of the associated depression and the fact that most of these patients undergo additional sugery after DH (such as cranioplasty, shunt implantation, etc.), we believe that the optimal time point to evaluate such patients should be at least 1 year after stroke. Of the patients in our study who underwent hemicraniectomy, 68.9% survived. These results are similar to those reported in other series [22, 25, 33, 34]. At 6 months after stroke, only 26.3% of survivors had a favorable functional outcome (mRS score B3). This percentage of good results is somewhat lower than that reported by Vahedi et al. [30]. Possible explanations for this discrepancy could be the limited number of patients in our study, the younger age of the patients in the study by Vahedi et al. [30], but most importantly, the fact that in Vahedi’s study, the mRS was evaluated at 1 year after stroke . Several studies have demonstrated that outcomes are poor in older patients [5, 9, 12, 14, 19, 28, 33, 34]. In the study by Holtkamp et al. [14], none of the patients aged more than 50 years achieved a BI score above 60 or a Rankin score below 4. All these patients were severely disabled and completely dependent upon others. When aggressive treatments are considered in any neurological disorder, the effects of treatment should be measured in terms of both survival and quality of survival. Consensus about the definition of QoL has yet to be
reached, but most researchers believe it is multidimensional [4]. In our study, the reduction in the overall QoL assessed by SIP was 38.2%. We observed a higher reduction in the physical domain than in the psychosocial domain. In patients with less severe stroke types (including subcortical and cortical infarctions, lacunar infarctions or intracerebral hemorrhages), a mean total SIP score of 23% 6 months after stroke has been reported [6]. Depressive symptoms are present in between 30 and 50% of patients with stroke [11, 15, 24, 27]. In MMCA infarction, these percentages are even higher [5, 33]. Carter et al. [5] found depressive symptoms in 9 of the 11 patients with malignant MCA infarction. Depressive symptoms were observed in 50% of our patients 6 months after injury. In two patients (12.5%), depression was severe. Our study is the first reporting neurobehavioral changes after space-occupying infarction, so our results cannot be compared. The most frequent negative symptoms, using the Frontal Behavioral Inventory (FBI), were decreased speech output, verbal apraxia, reduced spontaneity, apathy and inattention. The most frequent positive symptoms were impulsivity, irritability/disinhibition, perseveration, social inappropriateness, incontinence and poor judgment/ irresponsibility. Controversy surrounds the use of surgical treatment in patients with dominant hemispheric strokes for whom foreseeable aphasic sequels increase the potentiality for severe disability. Consequently, some authors are reluctant to consider patients with left-sided infarctions and complete aphasia candidates for DH [5, 7]. In our study, five patients showed dominant MMCA infarction. One patient had mixed transcortical aphasia, and even though the other four patients had global aphasia profiles, all of them
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preserved, to varying degrees, the ability to comprehend spoken language as well as some communication skills. Other studies have shown that the residual speech deficits in these patients are not as severe as expected, considering the large volume of affected brain [17, 22, 23, 33]. In agreement with Woertgen et al. [34] and Walz et al. [33], we found no differences in QoL or functional outcome between patients with left- or right-sided MMCA infarctions who underwent DH. Our results, although very preliminary, support the use of DH irrespective of which hemisphere is affected. When asked if they would undergo decompressive surgery again given the same outcome, 79% of the patients said yes, while 95% of the relatives reported they would again give consent. In contrast with the results of Foerch et al. [9], we found no relation between functional outcome measured by the BI and the retrospective agreement to undergo hemicraniectomy. Walz et al. [33] suggested that the perception of QoL depended not only on the degree of functional disability, but also on factors such as premorbid lifestyle and the personality of both patients and family members. Study limitations A potential limitation of this study is the fact that we did not include a comparison group of patients who did not have hemicraniectomy. As recent publications have provided level A evidence for recommending hemicraniectomy to reduce mortality in patients with MMCA infarction, all the patients of our hospital received this treatment option for ethical reasons. Other limitations of the study are the small sample size and the inbalance between dominant and non-dominant hemispheric infarctions. Although this inbalance could seem like a selection bias of our study, the distribution of right–left infarctions was in fact entirely due to chance.
Conclusions We can conclude from our study that DH reduces mortality and improves functional outcome in patients with MMCA infarction. Patients with favorable outcome are significantly younger. QoL seems to be acceptable in both leftand right-sided infarctions, and most patients and family members did not regret the decision to consent to DH. This observation raises an important issue that must be discussed in depth with patients and their families prior to the intervention, in terms of the extent to which the family members are willing to provide continuous assistance to a patient who will, in most cases, be left with severe deficits and will make them dependent in their daily life activities.
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J Neurol (2009) 256:1126–1133 Acknowledgments This study was supported by both the Fondo de Investigaciones Sanitarias de la Seguridad Social (FIS, grant no. 05/ 1092 received by Dr. J. Sahuquillo) and by the Fifth European Framework of the European Commission (SMILE project QLK1-CT2002-02583). Bessy Benejam was awarded a predoctoral research grant from the Institut Fundacio´ de Recerca Vall d’Hebron. We thank Dr. I. Bori and Dr. A. Amelivia from the Neurorehabilitation Department for taking care of the patients and for their continuous support of this study.
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