World J Urol (2014) 32:201–208 DOI 10.1007/s00345-013-1224-y
Diagnostic value of the pediatric lower urinary tract symptom score in children with overactive bladder Cem Akbal • Ahmet S¸ ahan • T. Emre S¸ ener Bahadır S¸ ahin • Ilker Tinay • Tufan Tarcan Ferruh S¸ ims¸ ek
Received: 8 October 2013 / Accepted: 5 December 2013 / Published online: 24 December 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Purpose The aims were (1) to assess the pediatric lower urinary tract symptom score (SS) prior to treatment as a means of determining severity of overactive bladder (OAB) and (2) to investigate relationships between SS results and those of standard diagnostic modalities. Materials and methods Symptom scores were recorded pre- and 6 months SS for 294 children with OAB unrelated to neurological disorder. Uroflowmetry–electromyography data, total bladder capacity, and a 2-day bladder diary were also recorded, and upper urinary tract deterioration was investigated as indicated. Overactive bladder was treated with standard approaches. No response to treatment was defined as 0–49 % reduction in OAB-related symptoms based on SS results. Non-responders underwent additional evaluations as indicated. Results Two hundred forty-one patients (97 %; mean age 9.8 ± 2.8 years; mean follow-up 11 months; range 6–18 months) completed the study. One hundred thirteen (47 %) required ultrasonography (USG), and those with abnormal USG had a significantly higher pre- and 6 months SS (p = 0.016). All non-responders (n = 38; 16 %) underwent urodynamics evaluation, 34 underwent spinal magnetic resonance imaging (MRI), 34 underwent voiding cystourethrography (VCUG), and 34 underwent
C. Akbal A. S¸ ahan T. E. S¸ ener B. S¸ ahin I. Tinay T. Tarcan F. S¸ ims¸ ek Pediatric Urology Division, Department of Urology, Marmara University School of Medicine, Istanbul, Turkey C. Akbal (&) ¨ roloji AD, Kat:4, Fevzi C¸akmak Mah. Mimar Sinan Cad, U ¨ niversitesi Eg˘itim ve Aras¸ tırma Hastanesi, Marmara U 34899 Pendik, Istanbul, Turkey e-mail: [email protected]
dimercaptosuccinic acid scanning (DMSA). Non-responders with terminal detrusor hyperactivity had significantly lower SS after therapy (p = 0.09). Non-responders with abnormal MRI had higher pre- and 6 months SS than those with normal MRI. Thirteen (38 %) of the non-responders who required VCUG had vesicoureteral reflux (VUR), and this subgroup had higher pre-treatment SS (p = 0.030). Seven (21 %) of the non-responders who required DMSA had scarring, and all 7 had VUR. The subgroup with scarring had higher pre-treatment SS (p = 0.030). Conclusion Pediatric OAB patients with high 6 months SS have a higher incidence of additional upper urinary tract pathology. Those with low pre-treatment SS require fewer laboratory tests and other assessments. The SS tool can reduce the number of urodynamics evaluations, and other tests required to diagnose renal damage in children with OAB. Keywords Symptom score Voiding dysfunction Treatment Ultrasonography Voiding cystourethrogram
Introduction Overactive bladder (OAB) is a common problem in the pediatric population. The reported prevalence of this condition in children 5–13 years of age ranges from 16.6 to 17.8 %, and prevalence has been shown to decrease with age [1–5]. History of cystitis and history of nocturnal enuresis are significantly associated with OAB in children . Constipation, fecal incontinence, delayed bladder control, and poor toilet facilities have also been identified as factors potentially associated with OAB in this age group [3, 4]. The International Children’s Continence Society (ICCS) has published a standardization document for diagnosing
lower urinary tract dysfunction in children . The diagnosis of OAB requires a series of steps: noninvasive screening through history taking, clinical examination, uroflowmetry, ultrasound, and a voiding diary. During case work-up for children with this condition, history is recorded from the parents and the child, and a structured approach involving a questionnaire is advised . Many signs and symptoms related to voiding and wetting are unknown to parents and should be specifically inquired about using a questionnaire instrument. In addition to being recommended for work-up, this method can help clinicians evaluate treatment outcome for these patients; however, to date, there has been no investigation of the efficacy of questionnaires for identifying the severity of OAB and predicting response to treatment in these children. The pediatric lower urinary tract symptom score (SS), originally developed and validated by Akbal et al.  (Fig. 1), is one of the most widely used scales for assessing dysfunctional voiding and has been applied in several studies [8, 9]. Other similar tools have also been used to assess these patients [10, 11]. The SS consists of 14 questions total, 13 related to lower urinary tract symptoms and one related to quality of life. Questions one and two inquire about daytime incontinence and questions three and four about enuresis nocturna. Four questions (numbers 5, 10, 11, and 12) gather data on filling-phase symptoms and five questions (numbers 6–9, 13) gather data on voiding symptoms. Question 14 is about quality of life . Our aims in this study were (1) to assess the value of pre-treatment SS findings for determining severity of OAB in children and (2) to investigate relationships between SS results and findings from standard diagnostic modalities used in this patient group.
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diagnosed with OAB unrelated to neurological disorder were enrolled in the study. Diagnostic testing The SS (Fig. 1) was administered to each patient and their parents at initial clinical evaluation (pre-treatment) and 6 months thereafter. For each patient, the pre-treatment SS and the 6 months SS were used for the study. Each patient underwent a combined uroflowmetry–electromyographic (EMG) assessment with the following parameters recorded: voided volume (mL), average flow rate (mL/s), peak flow rate (mL/s), post-void residual urine volume, EMG activity (positive or negative), and shape of the uroflowmetry curve [normal (bell-shaped), staccato, interrupted, or plateau, according to 2006 ICCS criteria] . Total bladder capacity [voided volume plus post-void residual urine volume measurement with ultrasonography (USG)] was expressed as a percentage of age-expected bladder capacity . Each patient completed a 2-day bladder diary with entries as per ICCS recommendations . Patients were eliminated from the study if their pre-treatment SS results did not match their bladder diary results. Subgroups of patients were assessed for deterioration of the upper urinary tract based on their symptoms. Those with mainly daytime symptoms, incontinence, and documented UTI underwent ultrasonography (USG) to assess for possible hydronephrosis. Those with confirmed UTI and abnormal urinary tract USG findings were assessed with voiding cystourethrography (VCUG), and vesicoureteral reflux (VUR) was graded according to the international classification [12, 13]. Children with VUR and/or abnormal USG findings plus confirmed UTI underwent a dimercaptosuccinic acid scan (DMSA), with results categorized as ‘‘normal’’ or ‘‘scarring present’’ .
Materials and methods Management protocol for overactive bladder Patients and diagnosis The subjects were children aged 4–17 years who were admitted to our Pediatric Urology Outpatient Clinic between February 2011 and February 2013 with one or more of the following symptoms: day–nighttime urinary incontinence, only daytime urinary incontinence, urinary urgency, weak stream, urinary hesitancy, increased urinary frequency, and urinary tract infection (UTI). Each child’s symptoms were recorded, and OAB was diagnosed if the patient met all three criteria’s: (1) sudden, imperative urinary urgency with or without urge incontinence; (2) need for holding maneuvers; (3) a minimum of seven small-volume urinations per day. Findings that supported the diagnosis of OAB were bladder capacity normal or low, and post-void residual urine volume \20 mL. Of all the children admitted, the 294 who were
Overactive bladder was treated with timed voiding regimens (patient with urge incontinence), anticholinergic medications (patient with urge and urge incontinence), and/ or antibiotics (patient with recurrent UTI with VUR). Patients with exclusively nocturnal symptoms were advised to limit fluid intake in the evening and to urinate before going to bed. Those with exclusively nocturnal symptoms resistant to initial treatment were prescribed oral desmopressin (DDAVP) or alarm therapy, as recommended in pediatric urology guidelines . Response to treatment, further testing ‘‘No response to treatment’’ was defined as 0–49 % reduction in OAB-related symptoms, which determined
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ahead of time based on pre- versus 6 months SS results . We treated the patients at least 6 months before categorized as non-responder. Patients with no response underwent additional diagnostic testing. Urodynamic evaluation All patients who did not respond to initial treatment were referred the urodynamics evaluation. A computerized urodynamics system was used to evaluate the lower urinary tract. Standard fluid cystometry was performed with the patient in supine position, using a 6F double-lumen urethral cystometry catheter and filling at 5–10 % of predicted bladder capacity per minute. The data recorded were as follows: bladder dynamics during the filling phase, detrusor leak point pressure (cmH2O), bladder compliance (mL/ cmH2O), bladder capacity (mL), abdominal pressure (cmH2O measured via rectal balloon catheter), and detrusor activity. Detrusor overactivity is an urodynamics observation characterized by involuntary detrusor contractions that are spontaneous or provoked during the filling phase and that raise detrusor pressure[15 cmH2O above baseline . Detrusor overactivity was categorized as phasic, non-phasic, or terminal .
Results Of the 294 total pediatric patients enrolled, 241 (82 %) completed the study. This group comprised 130 boys and 111 girls of mean age 9.8 ± 2.8 years (range 4–17 years). The median follow-up time was 6 months (range 3–18 months). The frequencies of presenting symptoms were as follows: 128 patients (53 %) reported nocturnal enuresis (plus imperative urinary urgency with or without urge incontinence, holding maneuvers and minimum of 7 small-volume urinations per day), 98 (41 %) reported nocturnal and daytime incontinence, and 15 (6 %) reported only daytime incontinence. Twenty-one patients (9 %) reported having encopresis in addition to enuresis. Two hundred three (84.3 %) of the 241 patients with OAB respond to treatment. The frequencies of presenting symptoms were not statistically different in both groups. The mean SS results for the responders (11.60 ± 6.24 vs. 5.04 ± 4.96 for pre-treatment and 6 months thereafter, respectively; p = 0.02). The ROC curve of pre-treatment symptom scores revealed that the score of the children reported as 23.5 or above less respond to the treatment. The specificity of the cutoff score of 23.5 was 93 %, but the sensitivity of the score of 23.5 was 30 % in our study group (Fig. 2).
Upper urinary tract deterioration
All patients who did not respond to initial treatment were referred the spinal magnetic resonance imaging (MRI). MRI was also performed in cases refractory to treatment. Findings of conus medullar is below the lower endplate of the L2 vertebra, lipoma or thickening of the filum terminales, and/or vertebral anomalies were considered abnormal. In addition to these evaluations, VCUG and DMSA were performed in non-responder cases as indicated.
Ultrasonography was indicated for 113 (47 %) of the 241 patients, and the results are shown in Table 1. The patients with abnormal USG results had a significantly higher mean pre-treatment SS than those with normal USG (17.6 ± 8.6 vs. 12.6 ± 7.4, respectively; p = 0.016). The mean 6 months SS results for these groups were not significantly different.
Thirty-eight (15.7 %) of the 241 patients with OAB did not respond to treatment. There was no significant difference between the mean pre- and 6 months SS results for the non-responders. All 38 of these patients underwent urodynamic evaluation, 34 underwent spinal MRI, 34 with confirmed UTI underwent VCUG, and 34 with abnormal USG underwent DMSA.
Findings for pre- and 6 months SS were compared. Data were analyzed using the Statistical Package for the Social Sciences (SPSS version 20, IBM Corporation, NY, USA). Univariate analysis was performed using the independentsamples Student’s t test and Fisher’s exact test. The pairedsamples Student’s t test was used to compare means for variables of interval scale. Fisher’s exact test was used to analyze categorical data. P values \ 0.05 were considered significant. Receiver operating characteristic (ROC) plots were used to define detection cutoff or threshold score, and Youden’s index was used to detect best reflecting optimal sensitivity and specificity .
Findings after additional testing
Urodynamic results Of the 38 patients who underwent urodynamic assessment, 13 exhibited phasic detrusor overactivity, 12 terminal detrusor overactivity, eight normal detrusor activity, and five non-phasic detrusor overactivity (Table 1). Both these groups had significantly lower mean SS after treatment, and
World J Urol (2014) 32:201–208 1.
Does your child have urinary incontinence (peeing while not on the toilet) during the day? If Yes to Question 2
Does your child have urinary incontinence (peeing while not on the toilet) during the night?
3 or more times/day
A few drops
Only underwear wet
Outer clothing layers wet
If Yes to Question 4 …
Underwear or pajamas wet
Less than 7 times/day
7 or more times/day
11. My child can hold his/her pee by crossing his/her legs, squatting, or doing the “pee dance.’’
12. My child wets his/her clothes before reaching the toilet.
My child goes to the toilet to pee …
5 Bed wet
My child has to strain to pee.
My child experiences pain when s/he pees.
My child pees intermittently when on the toilet.
My child has to go to revisit the toilet to pee soon after s/he pees.
10. My child has to run to the toilet when s/he feels the need to pee.
13. My child does not pass stool every day.
QUALITY OF LIFE If your child experiences any of the symptoms/issues mentioned above, does this affect his/her family life or social life?
Fig. 1 Pediatric lower urinary tract symptom score
Not at all
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cord, 2 lipoma) (Table 1). Both these subgroups had significantly lower mean SS after treatment, and the mean SS results for the non-responders with normal MRI (10.9 ± 4.7 vs. 8.7 ± 4.6 for pre- and 6 months SS, respectively; p = 0.032) were lower than those for the nonresponders with abnormal MRI (27.6 ± 6.1 vs. 21.5 ± 11.1, respectively; p = 0.026) (Table 1). Area under ROC curve for patients with abnormal findings by trapezoidal rule was 0,974, and threshold score was 16 (sensitivity 92 %, specificity 86 %). Other test results
Fig. 2 Area under ROC curve for patients by trapezoidal rule was 0,974, and threshold score was (sensitivity 23.5 %, specificity 93 %)
the mean SS results in the non-responders with normal urodynamics (12.8 ± 13.4 vs. 11.5 ± 12.88. for pre- and 6 months SS, respectively; p = 0.032) were lower than those in the non-responders with abnormal urodynamics (20.6 ± 9.1 vs. 15.6 ± 10.9, respectively; p = \0.001 (Table 1).
Table 1 lists the result for the subgroups that required VCUG and DMSA, respectively. Of the 34 non-responders who required VCUG, 26 (76 %) were girls and 8 (24 %) were boys. Thirteen (38 %) of these 34 children were diagnosed with VUR on VCUG. The non-responders with VUR had a significantly higher mean pre-treatment SS than those without VUR (20.8 ± 9.7 vs. 13.6 ± 9.4, respectively; p = 0.030) (Table 1). Of the 34 non-responders who required DMSA, 29 (85 %) were girls and 5 (15 %) were boys. Seven (21 %) of these 34 patients had scarring, and these individuals were all diagnosed with VUR on VCUG. The mean pretreatment SS was significantly higher in non-responders with abnormal DMSA scans than in those with normal scan results (17.8 ± 10.5 vs. 11.5 ± 10.6, respectively; p = 0.030) (Table 1).
Of the 34 children who underwent spinal MRI (4 patients did not accept MRI evaluation), 21 (62 %) had normal findings and 13 (38 %) had abnormal findings (11 tethered
Our main findings were that children with OAB who did not respond to treatment (i.e., those with more severe OAB) had higher pre-treatment SS than treatment
Table 1 Demographics and symptom score results for the non-responders with normal and abnormal test results No. of patients (%)
24 (66 %)
12 (33 %)
8.4 ± 2.2
8 (21 %)
8.5 ± 2.1
30 (79 %)
8.5 ± 2.4
20.6 ± 9.1
Normal DA Abnormal DA
Age (years) 9.2 ± 2.2
p value (paired-samples t test)
14.3 ± 6.4
10.4 ± 7.8
20.5 ± 9.2
15.6 ± 9.2
12.8 ± 13.4
11.5 ± 12.8
15.6 ± 10.9
21 (62 %)
8.2 ± 1.8
10.9 ± 4.7
8.7 ± 4.6
13 (38 %)
8.6 ± 2.6
27.6 ± 6.1
21.5 ± 11.1
Normal VCUG Abnormal VCUG
21 (62 %) 13 (38 %)
8.3 ± 1.8 8.3 ± 2.3
13.6 ± 9.4 20.8 ± 9.7
12.0 ± 9.8 12.3 ± 9.6
27 (79 %)
8.37 ± 2.1
11.5 ± 4.6
8.1 ± 3.4
7 (21 %)
8.29 ± 1.6
17.8 ± 10.5
13.1 ± 10.6
F female, M male, SS symptom score, USG ultrasonography, DA detrusor activity, MRI magnetic resonance imaging, DMSA dimercaptosuccinic acid scan, VCUG voiding cystourethrography
responders and tended to have abnormal results on other diagnostic tests. Approximately 16 % of our 241 children with OAB were resistant to treatment. Urodynamic assessments of these 38 patients revealed that 30 had abnormal fillingphase cystometry. We did not perform urodynamic testing on initial evaluation, as previous studies have suggested . Glassberg et al.  recommended urodynamics evaluation for several pediatric patient groups: those with a combination of lower urinary tract dysfunction and history of febrile UTI presenting after toilet training; those with impaired flow despite a quiet pelvic floor on repeated flow/ EMG studies; those with lower urinary tract dysfunction associated with marked bladder wall thickening, hydronephrosis, or lower ureteral dilatation on ultrasound; those resistant to empirical or standard therapy (i.e., timed voiding, anticholinergic therapy, and/or biofeedback). In our study, we found that mean pre- and 6 months SS results were statistically different for non-responders with either normal or abnormal urodynamics findings. This suggests that, for children who have undergone first-line OAB therapy, high 6 months SS might indicate presence of urodynamics abnormality. We found indications for spinal MRI in 34 of the 241 patients who did not respond to OAB treatment, and 13 (38 %) of these 34 children had abnormal MRI findings. These patients with abnormal MRI had a statistically higher mean 6 months SS than patients with normal MRI. Our findings suggest that pediatric OAB patients who are resistant to treatment and have abnormal urodynamics may have some degree of spinal pathology and, thus, should undergo spinal MRI. Such patients should be evaluated by a pediatric neurosurgeon. Pippi Salle et al.  evaluated 32 consecutive children with complicated enuresis who were referred for neurosurgical evaluation. They recorded normal spinal MRI findings in 21 patients (91.3 %), including one with a tethered cord and lipoma associated with a complex skeletal abnormality, and one with a nonprogressive, non-surgical syrinx extending from T7 to T9 spinal levels. Only the case of lipoma required neurosurgical intervention. The authors concluded that MRI is of limited value in children with voiding dysfunction who have a normal neuro-orthopedic assessment and that this modality should be reserved for those with associated neuro-orthopedic findings or complex skeletal deformity on plain X-ray . In contrast, Arikan et al.  investigated 81 children with voiding dysfunction and reported pathologic findings in 17 (38.6 %) of 44 patients who had a normal neuroorthopedic assessment. They concluded that MRI of the lower spinal cord is a valuable tool for diagnosing occult spinal cord disorders, particularly in patients with the combination of voiding dysfunction refractory to
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conservative management and normal neurological and orthopedic assessment. There was a marked difference in symptom scores of children who had spinal pathology and those voiding dysfunction without spinal pathology. In our current study, the threshold score was 16 (sensitivity 92 %, specificity 86 %). Unfortunately, the specificity of the cutoff score of 23.5 was 93 %, and the sensitivity of the score of 23.5 was 30 %, respectively. This sensitivity was not as high as MRI positive patients. This shows that the symptom scores can only differentiate the specific subgroups as spinal pathology in non-responders. We recommend VCUG for children with combined lower urinary tract dysfunction and history of febrile UTI who have high 6 months SS because they are refractory to conservative management. In the series reported by Glassberg et al. , 19 (33 %) of 57 patients with OAB had VUR, and 32 (56 %) had UTI. Similarly, we found that 38 % of our non-responder patients had VUR. Pelvic floor overactivity and involuntary detrusor contraction have been linked with occurrence of UTI in children . Strong contraction of the proximal urethra and pelvic floor muscles against involuntary detrusor contraction might cause UTI. This condition can lead to urethrovesical reflux of bacteria in the proximal urethra [20, 21]. Sille´n et al.  conducted a ‘‘reflux trial’’ in Swedish children, which evaluated lower urinary tract dysfunction in 161 pediatric patients with dilating reflux. The authors observed isolated OAB in 15 (9 %), voiding phase problems in 39 (24 %), and a negative correlation between dysfunction at 2 years and improved dilating reflux . Renal damage at study entry and follow-up was associated with lower urinary tract dysfunction at 2 years . Recurrent UTI was observed in 33 and 20 % of the children with and without voiding dysfunction, respectively (p = 0.084) . In our study sample, 5.4 % of 241 children with OAB had VUR. The sample in the Swedish reflux trial differed from ours with respect to age; however, other comparable studies with wider patient age range have reported similar results [1, 22–24]. Many children with voiding phase problems also have OAB symptoms . Some children in our study might have had voiding phase disorders in addition to OAB; however, recent investigations of renal damage in patients with OAB have noted rates of lower urinary tract dysfunction, including OAB, comparable to ours [26–28]. Twenty-one percent of our 34 non-responders who underwent DMSA had renal scarring. According to the Swedish reflux trial, renal damage at study entry and follow-up was more common in children with lower urinary tract dysfunction than in children with normal lower urinary tract function . However, the trial authors found no statistical difference regarding presence of renal damage between children with isolated OAB and those with
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voiding phase problems . One explanation for this might be that patients in their series had younger and less UTI attack during their life time period. Our study has limitations. Our study did not include a control group. Since we did not perform urodynamics evaluations for all patients with OAB at initial evaluation, the bladder dynamics of those who responded to treatment were unknown. Although we establish a specific SS result that would be a cutoff (23.5) for identifying patients who require evaluation with invasive methods, the only value that seems to be significant was specificity of the cutoff score. We did not correlate the treatment intensity with SS. Finally, we did not correlate the SS with initial uroflowEMG study. We used the uroflow-EMG for support the diagnosis the OAB. The SS is a simple noninvasive means of evaluating pediatric patients with lower urinary tract dysfunction and following their response to treatment. To our knowledge, ours is the first study to have assessed relationships between SS results and those of invasive diagnostic tests for children with OAB. Our findings suggest that high preor 6 months SS in this patient group might indicate presence of additional pathology; however, cutoff values for SS are needed in order to identify those who require invasive diagnostics. Our results also indicate that patients with low SS need fewer laboratory tests or other noninvasive assessments and that a finding of low SS also helps establish a diagnosis of lower urinary system dysfunction. Use of the SS could reduce the number of urodynamics evaluations, and other tests required to reach a diagnosis of upper urinary tract deterioration in patients with OAB. This result is in accord with our own clinical experience to date; however, more studies are needed to investigate the clinical use of SS more thoroughly.
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