Pediatric Urology
Evaluation of a New Ultrasound Measurement
Tool for the Diagnosis of Dysfunctional
Voiding in Pediatric Population: Full/Empty
Bladder Wall Thickness Ratio
Semih Tangal, Mehmet _Ilker G
€okc¸e, Asım €Ozayar, Bas¸ak G€ulpınar, Ahmet Hakan Haliloglu,
Berk Burgu, and Erol €
Ozdiler
OBJECTIVE To investigate the roles of bladder wall thickness (BWT) measurement and full/empty (F/E) BWT measurement ratio in the diagnosis of dysfunctional voiding in pediatric population. METHODS Totally, 324 patients were involved in this prospective study, and group 1 consisted of healthy
children (n ¼ 198), and group 2 consisted of patients with dysfunctional voiding (n ¼ 126). BWT measurements were done at the anterior, posterior, and lateral walls, and F/E BWT ratios were calculated. Two groups were compared for BWT measurement, and receiver operating characteristic analysis was performed tofind out a cutoff value for BWT and F/E BWT ratios. RESULTS Mean age of group 1 was 6.4 years and that of group 2 was 6.5 years. BWT measurements were
higher in the empty state compared with full state and in boys compared with girls. However, BWT ratios did not show significant difference between male and female patients. F/E BWT ratios were found to be higher in group 2 compared with group 1 (P¼ .02). In receiver operating characteristic analysis, a cutoff value of 0.324 (sensitivity 66.67% and specificity 79.80%) and 0.295 (sensitivity 83.33% and specificity 64.14%) was found for anterior and posterior F/E BWT rates, respectively. CONCLUSION Ultrasonographic measurement of BWT and calculation of F/E BWT ratio may serve as a non-invasive tool for evaluating lower urinary tract symptoms in children. Further studies including larger number of patients would be of great interest. UROLOGY83: 1369e1372, 2014. 2014 Elsevier Inc.
I
n children, lower urinary tract symptoms (LUTS) including dysfunctional voiding and neurogenic bladder may result in increased intravesical pressure and bladder wall hypertrophy.1,2Changes in morphology and function of the lower urinary tract are generally evaluated with urodynamic investigations, which are invasive and time consuming. Because urodynamic tests cause a significant stress on both children and their par-ents, affectivity of noninvasive methods including ultra-sound scan (US) in diagnosing LUTS has been investigated in previous studies.2-5Bladder wall hypertrophy is caused by the thickening of the detrusor with increased collagen deposition in the bladder wall.6Bladder wall thickness (BWT) reflects the workload of the bladder, and US emerged as
the simplest and noninvasive method in measuring BWT.1,4 In previous studies, BWT measurements by US have been shown to have similar affectivity to those of urodynamic tests in the differential diagnosis of LUTS.1,7,8 A structured way of investigating LUTS by US may potentially help clinicians to plan a proper management and objectively evaluate the outcomes of the treatment.
In this study, we aimed to generate a clinically useful ultrasonographic tool to identify the impaired elasticity of bladder wall of children with LUTS. Because BWT measurements using US reveal great diversity in children, we hypothesized that the individual ratio of full/empty (F/E) BWT may help to identify a cutoff value to differ-entiate children with LUTS from healthy controls.
MATERIALS AND METHODS
The study was performed between February 2008 and March 2010. Informed consent was taken from the families of children who were enrolled into the study. Patients were grouped into 2 groups. Group 1 consisted of healthy children from a primary public school in Ankara, Turkey, and group 2 consisted of children diagnosed and followed up with the diagnosis of dysfunctional voiding (based on voiding dysfunction symptom
Financial Disclosure: The authors declare that they have no relevantfinancial interests. From the Department of Urology, Ufuk University, School of Medicine, Ankara, Turkey; the Department of Urology, Ankara University, School of Medicine, Ankara, Turkey; the Department of Urology, Atat€urk Training and Research Hospital, Ankara, Turkey; and the Department of Radiology, Ankara University, School of Medicine, Ankara, Turkey
Reprint requests: Mehmet _Ilker G€okc¸e, M.D., Ankara Üniversitesi Tıp fakultesi €uroloji A.D. _Ibni Sina Hastanesi, Sıhhıye 06590, Ankara, Turkey. E-mail:migokce@ yahoo.com
Submitted: November 26, 2013, accepted (with revisions): December 26, 2013
ª 2014 Elsevier Inc. 0090-4295/14/$36.00 1369
score [VDSS]). VDSS was previously used in the study of Akbal et al.9Children were between the ages of 5 and 10 years. All patients were prospectively involved into the study. Detailed history and physical examination, including neurologic examination, were performed in all children. VDSS question-naire was given to all patients in both groups to evaluate the presence of voiding dysfunction. Urinary US, urinalysis with a dipstick, uroflowmetry, and residual urine measurements were performed in all children, and urine cultures were performed in case of suspicious infection on the basis of the results of urine analysis. Uroflowmetric and ultrasonographic tests were evalu-ated by the same physicians who were blind to the outcomes of other measurements included in the study.
Ultrasonographic evaluation of the bladder was performed with high frequency (7.5 MHz) linear probe in supine position from suprapubic region. The measurement of BWT was performed by the same physician when the child had a strong desire to void and after micturition. BWT measurements were performed using the technique previously described by M€uller et al.10
BWT was assessed by measuring the distance between 2 hyperechogenic lines, which represent the adventitia and mucosa and/or submu-cosal tissue, respectively.1The anterior wall was measured at the lateral aspect of the urachus, the posterior wall was measured where the rectal impression was present, and lateral walls were measured at both the lateral sides of the bladder.2,3BWT
mea-surements were performed from anterior, posterior, and 2 lateral walls separately both at full and empty stages, and ratios of mea-surements at full and empty stages (F/E ratio) were calculated.
Uroflowmetric patterns other than bell-shaped were accepted as abnormal. Uroflowmetry was repeated in children with an abnormal pattern at the initial test, and the children with abnormal voiding in 2 repeated tests were accepted as abnormal voiders. Children with positive nitrite and leukocyte esterase measurements in the dipstick urine test were accepted to have urinary tract infection, and urine cultures were performed. Children were evaluated after treatment of infection with appropriate antibiotics based on urine cultures.
Statistical Analyses
Statistical analyses were performed with SPSS 15.0, and the statistical significance was set as P <.05. Because the parameters
evaluated in the study did not have a normal range because of Kolmogorov-Smirnov analyses, Bonferroni-corrected Kruskal-Wallis test was used to compare the medians. Receiver operating characteristic (ROC) analyses were performed to find out a cutoff value for F/E BWT rate in the differential diagnosis of dysfunctional voiding.
RESULTS
There were 198 children (male/female: 122/76) in group 1 and 126 children (male/female: 75/51) in group 2. Mean age was 6.4 years in group 1 and 6.5 years in group 2, and the difference was not statistically significant (P ¼ .84). In group 1, BWT measurements were found to be signi fi-cantly higher in boys compared with girls in both empty and full bladder stages. However, F/E ratios were not found to be significantly different. In group 2, BWT measure-ments were found to be significantly higher in boys compared with girls when the bladder is empty. However, BWT measurements when the bladder is full and F/E ratios were not found to be significantly different. The results of BWT measurements are summarized inTable 1. F/E ratios did not show significant difference within the groups based on sex; therefore, F/E ratios of the entire groups from 4 different walls were compared. F/E ratios were significantly higher in all the 4 different wall mea-surements in group 2. The results of F/E ratios are sum-marized inTable 2.
Owing to the wide range of BWT measurements with ultrasonography, a cutoff value for normal range of BWT could not be detected. To diagnose dysfunctional voiding, a cutoff value of 0.324 (sensitivity 66.67% and specificity 79.80%) and 0.295 (sensitivity 83.33% and specificity 64.14%) was found for anterior and posterior F/E BWT rate, respectively with ROC analyzes.
COMMENT
Dysfunctional voiding has an increasing prevalence in children. It has important consequences on quality of life
Table 1. Bladder wall thickness measurements of the 2 groups from 4 different bladder walls
Measurement
Group 1 Group 2
Male Female P Value Male Female P Value
Anterior wall Empty (mm) 3.9 (3.1-6.2) 3.55 (3.3-6.1) .03 4.2 (3.5-6.3) 3.9 (3.1-5.9) .04 Full (mm) 1.2 (0.7-2.1) 1.1 (0.7-2.2) .04 1.5 (0.9-2.8) 1.4 (0.9-2.6) .07 F/E ratio 0.292 (0.189-0.4) 0.305 (0.194-0.38) .85 0.340 (0.243-0.47) 0.358 (0.257-0.46) .81 Posterior wall Empty (mm) 3.8 (3-6) 3.5 (3-6) .04 4.2 (3.5-6.1) 3.8 (3-6) .04 Full (mm) 1.1 (0.7-2) 1 (0.6-2.2) .04 1.4 (0.9-2.7) 1.3 (0.9-2.7) .06 F/E ratio 0.282 (0.216-0.37) 0.279 (0.2-0.367) .88 0.333 (0.243-0.45) 0.330 (0.257-0.45) .86 Right lateral wall
Empty (mm) 3.9 (3-6) 3.5 (3.2-6) .03 4.2 (3.4-6.2) 3.9 (3-5.9) .03 Full (mm) 1.1 (0.7-2) 1.05 (0.7-2.1) .04 1.5 (0.9-2.7) 1.3 (0.9-2.7) .06 F/E ratio 0.277 (0.194-0.38) 0.285 (0.212-0.38) .84 0.326 (0.243-0.46) 0.342 (0.257-0.45) .74 Left lateral Empty (mm) 3.9 (3.1-6.2) 3.5 (3.1-6) .04 4.2 (3.4-6.2) 3.9 (3-5.9) .04 Full (mm) 1.1 (0.7-2) 1(0.6-2) .04 1.5 (0.9-2.7) 1.3 (0.9-2.7) .06 F/E ratio 0.282 (0.194-0.40) 0.285 (0.171-0.38) .92 0.325 (0.243-0.4) 0.342 (0.257-0.46) .89
F/E ratio, full/empty bladder wall thickness ratio. Data presented as mean (range).
of both children and their parents. Therefore, diagnosis and proper treatment of dysfunctional voiding are important issues. Diagnosis of dysfunctional voiding mainly relies on voiding questionnaires and uroflowmetry but videourodynamic evaluation may be needed for diagnosis but it is invasive and expensive besides requires special equipment and trained personnel. Radiation exposure is another disadvantage.4 Therefore, develop-ment of less invasive diagnostic tools is mandatory, and voiding diaries, questionnaires, and uroflowmetry are currently used as diagnostic methods together with US.
US is being used with increasing frequency for the diagnosis of dysfunctional voiding, with the advantages of being noninvasive, rapid, simple, and cheap. Oelke1 mentioned that bladder wall imaging might be helpful to understand disease development or predict treatment outcome, and it was previously advocated that BWT measurements with US have the potential to replace urodynamic evaluations in the diagnosis of dysfunctional voiding.1,11 However, although it is a simple and cheap method, it has a low specificity for the evaluation of dysfunctional voiding.
BWT assessed with US reflects the workload of the bladder.1 The bladder wall appears on US as a 3-layer structure with the detrusor muscle represented by a hypo-echogenic layer between 2 hyperhypo-echogenic layers, which represent serosa and mucosa, respectively.1 In different studies, the thickness of the 3 layers together or only the middle detrusor layer has been measured.7,12Similarly, some investigators used the anterior bladder wall for measure-ments, whereas others preferred to use the posterior wall.4,13 Previous studies have demonstrated no significant differ-ences in the thickness of the various parts of the bladder wall.5,14In this study, BWT measurements were performed in different parts of the bladder wall, including anterior, posterior, and lateral walls, and the effect of gender on BWT measurements was also assessed. It was previously suggested that it is necessary to use high frequency ultrasound arrays (7.5 MHz or higher) for precise measurement of BWT.12In our study, BWT measurements were performed by a single experienced radiologist with a 7.5 MHz US instrument.
It was previously demonstrated that the BWT decreases with increasingfilling volume.2,4,12Similar to these trials,
BWT at empty bladder was higher compared with full bladder in all groups for all measurements in the recent study. We have observed that boys had thicker bladder walls at anterior, posterior, and lateral aspects, and this was in accordance with previousfindings.3Thisfinding can be explained by high urethral resistance and high voiding and maximum detrusor pressure in boys.3,15However, F/E BWT ratio did not show any difference between the genders. There are limited studies evaluating BWT of healthy children and children with dysfunctional voiding.16,17In one of these studies it has been shown that children with abnormal urodynamics pattern had thicker bladder walls.16 In another study, children with dysfunctional voiding because of meningomyelocele and healthy chil-dren were included, and no significant difference was noted for BWT measurements between the 2 groups.17
In our study, BWT measurements of children with dysfunctional voiding were significantly higher than normal children for both full and empty bladder. How-ever, because of the great diversity of BWT measure-ments, it was not possible to find out a cutoff value for diagnosis of dysfunctional voiding. Therefore, F/E bladder BWT ratios were calculated and compared. This ratio was significantly higher in children with dysfunctional void-ing compared with healthy children. Those findings can be explained with decreased expansion capacity of the bladder because of collagen reformation at bladder wall in children with dysfunctional voiding.
Measurement of BWT alone seems to have a low correlation with presence or degree of dysfunctional voiding. Besides, it is shown to be gender dependent. Effect of dysfunctional voiding on BWT is based on loss of capacity becoming slimmer while the bladder is getting full. Therefore, calculating the ratio of full and empty BWT may be a good way of evaluating the status of bladder wall. In our study, cutoff values of 0.324 and 0.295 with slightly low sensitivity and specificity were found for anterior and posterior F/E BWT rate respec-tively with ROC analyzes. Although these results are insufficient to conclude use of a cutoff level for F/E BWT, they are promising for further research combining use other noninvasive diagnostic methods together with ul-trasonographic BWT measurements for the exact diag-nosis of dysfunctional voiding in children.
CONCLUSION
Ultrasonographic measurement of BWT and calculation of F/E BWT ratio may serve as a noninvasive tool for evaluating LUTS in children. Further studies including larger number of patients would be of great interest.
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Table 2. Comparison of the full/empty bladder wall thickness ratios of the 2 groups
Measurement Group 1 Group 2 P Value Anterior wall F/E ratio 0.295 (0.189-0.4) 0.349 (0.243-0.47) .02 Posterior wall F/E ratio 0.282 (0.2-0.372) 0.333 (0.243-0.45) .03 Right lateral wall F/E ratio 0.279 (0.194-0.38) 0.336 (0.243-0.47) .02 Left lateral wall F/E ratio 0.281 (0.171-0.40) 0.328 (0.243-0.47) .03 Abbreviation as inTable 1. Data presented as mean (range).
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