Lower Urinary Tract Conditions in Children With Attention Deficit Hyperactivity Disorder: Correlation of Symptoms Based on Validated Scoring Systems

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1 Lower Urinary Tract Conditions in Children With Attention Deficit Hyperactivity Disorder: Correlation of Symptoms Based on Validated Scoring Systems Berk Burgu, Ozgu Aydogdu,* Kagan Gurkan, Runa Uslu and Tarkan Soygur From the Department of Urology (BB, OA, TS), and Department of Child and Adolescent Psychiatry (KG, RU), Ankara University School of Medicine, Ankara, Turkey Purpose: We investigated whether certain voiding problems have a higher incidence in patients with attention deficit disorder with hyperactivity compared to age matched controls. Materials and Methods: We used the Conners Parent Rating Scale-revised for attention deficit disorder with hyperactivity and lower urinary tract symptom score to evaluate voiding problems. A total of 62 children with attention deficit disorder and 124 healthy controls were enrolled. We evaluated uroflowmetry patterns in both groups. Residual urine volumes and Bristol stool scale were noted. We examined the correlation between total Conners Parent Rating Scalerevised and lower urinary tract symptom score in patients with attention deficit disorder. Additionally we analyzed each index of the Conners Parent Rating Scale-revised separately in terms of correlation with symptom subgroups for lower urinary tract symptom scores. Results: Mean SD total lower urinary tract symptom score was in patients with attention deficit disorder with hyperactivity and in controls, a difference that was statistically significantly (p 0.001). With the exception of constipation, mean scores of all lower urinary tract symptom subindices were significantly higher in patients with attention deficit disorder compared to controls. Symptoms evaluated in lower urinary tract symptom score were mostly correlated with attention deficit disorder index of the Conners Parent Rating Scale-revised. If a child with attention deficit disorder has a high index in the Conners Parent Rating Scale-revised, he or she is more likely to have urgency. Also, if a child with attention deficit disorder has a high hyperactivity subscale score, he or she is more likely to have enuresis. Conclusions: Voiding problems are more common in children with attention deficit disorder with hyperactivity than in age matched controls. Urgency and enuresis are the outstanding problems in children with attention deficit disorder. Simultaneous use of the Conners Parent Rating Scale-revised and lower urinary tract symptom score questionnaire should be encouraged in patients with attention deficit disorder to allow a structured and quantitative evaluation of these overlapping problems. Abbreviations and Acronyms ADHD attention deficit disorder with hyperactivity BSS Bristol stool scale CPRS Conners Parent Rating Scale CPRS-R Conners Parent Rating Scale-revised LUT lower urinary tract LUTSS lower urinary tract symptom score UFM uroflowmetry Submitted for publication May 7, * Correspondence: Department of Urology, Ankara University, Adnan Saygun cad Altındağ, Ankara, Turkey (telephone: ; FAX: ; ozgucan@ yahoo.com). Key Words: attention deficit disorder with hyperactivity; enuresis; urinary bladder, overactive ACCORDING to the Diagnostic and Statistical Manual of Mental Disorders, attention deficit disorder with hyperactivity is defined by symptoms of inattention, hyperactivity and impulsivity that are present in at least /11/ /0 Vol. 185, , February 2011 THE JOURNAL OF UROLOGY Printed in U.S.A by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC. DOI: /j.juro

2 664 LOWER URINARY TRACT CONDITIONS IN CHILDREN WITH ATTENTION DEFICIT DISORDER different settings for 6 months before age 7 years. 1 3 Many studies have stressed the comorbidity between lower urinary tract dysfunction, especially enuresis, and attention deficit disorder. 1 6 The cooccurrence of enuresis and attention deficit disorder is about 30%. 3,7 Associated LUT problems adversely affect patient sense of well-being and psychosocial functioning, which can already be decreased in a child with ADHD Therefore, diagnosis and management of ADHD and concomitant LUT problems are major issues in clinical practice. 11 The Conners Parent Rating Scale is a common comprehensive rating tool for acquiring parent reports on basic problems. 12 CPRS contains items evaluating the whole psychosocial status of the child. It also includes items covering the cardinal symptoms of ADHD, ie inattention, hyperactivity and impulsivity. 11,12 The Conners scale used in this study was revised by Conners et al. 13 The reliability and validity of the Turkish version of the scale were studied by Kaner et al. 14 Symptom scoring systems are widely used in pediatric urology. Although they cannot replace diaries, they provide a structured evaluation. LUTSS is a validated example that is frequently used. 15 In our prospective study we compared LUTSS results of children with ADHD and age matched controls. We also investigated whether there is any correlation between CPRS-R and LUTSS in the assessment of ADHD and potential comorbid bladder dysfunction. PATIENTS AND METHODS The CPRS has been widely used in clinical and epidemiological studies, and assesses the co-occurrence of the important symptoms of ADHD. In this series items were noted by parents on a 4-part answer scale ranging from 0 for not at all true to 3 for very much true. The CPRS contains 80 items and covers a subset of evaluation scales, including oppositional, cognitive problems/inattention, hyperactivity and ADHD indices. 12,16 Parents of all patients with ADHD completed the CPRS-R. The LUTSS questionnaire was also answered by all parents, evaluating 5 main symptom groups, including enuresis, constipation, urgency, holding maneuvers, and voiding and other symptoms. A total of 28 boys and 34 girls 6 to 17 years old with ADHD and 124 healthy controls (68 boys and 56 girls 7 to 15 years old) were evaluated with LUTSS. ADHD diagnoses were made by a child and adolescent psychiatrist based on DSM-IV-TR criteria. 1 Voiding patterns in both groups were evaluated with uroflowmetry performed twice. To obtain a standard measurement and be concordant with the literature, all uroflow tests were performed at strong desire to void. Residual urine volumes were also examined by bladder scan (BladderScan BVI 6100). Voiding curves were classified as bell, tower, plateau, staccato and interrupted. All patterns but bell-shaped patterns were considered abnormal. Six patients in the control group with 2 diverse voiding curves were excluded from the study. To evaluate fully the bowel status, the BSS was used in both groups. All families of children with ADHD and age matched healthy controls were given a 3-day bladder diary documenting voiding frequency, day and time of urine output, incontinence and enuresis. Bladder diaries with a voiding frequency above 8 or below 3, incontinence or enuresis were considered abnormal. Total LUTSS were compared between patients with ADHD and controls. Two groups were also compared in terms of UFM patterns, residual urine and constipation. Patients who had stool types of 1 or 2 according to BSS were considered constipated. 17 In patients with ADHD correlation between total CPRS-R and LUTSS was examined. Same analyses for subgroups according to gender and age were also performed. In patients with ADHD correlation of subscale scores of CPRS-R scale with total LUTSS scores was analyzed. Same correlation analyses between 5 LUTSS subindices and total CPRS-R were also performed. Each subscale score of CPRS-R was separately analyzed in terms of correlation with symptom subgroups of LUTSS. In the ADHD group the correlation of total LUTSS and CPRS-R and subindices of each scoring system was evaluated using Spearman s rho test for gender and 3 separate age groups (6 to 10, 10 to 13 and 13 to 17 years old). Voiding patterns were compared for gender and age groups using chi-square test. UFM patterns were also examined for total and subscale scores of CPRS-R by Kruskal-Wallis test. Same analyses were made for residual urine volumes by Mann-Whitney U test. UFM patterns and residual urine volume measures were also compared between ADHD and control groups by chi-square test. Statistical significance was set at p RESULTS ADHD vs Control Mean total LUTSS in patients with ADHD was significantly higher than in controls (table 1). Mean scores of all LUTSS subindices, except constipation, were significantly higher in the ADHD group. Non- Table 1. LUTSS in patients with ADHD and controls ADHD Group Controls p Value Mean SD LUTSS: Nocturnal enuresis Constipation Urgency Holding maneuvers Voiding other symptoms % UFM patterns: Bell shaped Nonbell shaped % Residual urine vol: Significant Not significant

3 LOWER URINARY TRACT CONDITIONS IN CHILDREN WITH ATTENTION DEFICIT DISORDER 665 bell-shaped UFM pattern and significant residual urine volumes were significantly higher in patients with ADHD than in age matched controls. The most common voiding pattern for both groups was bell shaped (table 1). The second most common pattern for the ADHD group was staccato (24.2%), which was not correlated to gender, age or CPRS-R subscale. Constipation did not differ between the 2 groups (p 0.54). The percentage of abnormal voiding diaries was significantly higher in the ADHD population (22%) than in controls (5%). Gender and Age For patients with ADHD total LUTSS and CPRS-R were not correlated (p 0.087). However, when further analysis was performed regarding gender, a significant positive correlation was noted between total CPRS-R and LUTSS in males (p 0.05, correlation coefficient r 0.37). Total CPRS-R of females was not correlated to LUTSS. When effect of age was evaluated, only patients with ADHD who were 6 to 10 years old had a positive correlation between total LUTSS and CPRS-R (p 0.046, r 0.32). For the older groups no correlation was observed. Since the CPRS-R is generally used by evaluating subindices such as ADHD index, cognitive problems/inattention, hyperactivity and oppositional rather than total scores, further evaluation according to subindices was performed. Analyses of Lower Urinary Tract Symptoms When specific symptoms on LUTSS questionnaires of patients with ADHD were examined, males had significantly higher enuresis (p 0.001) and constipation (p 0.001), while females had significantly higher urgency (p 0.006) and holding maneuvers (p 0.001). When total LUTSS and subindices of patients with ADHD were evaluated for age, no statistically significant difference was found. Mean total LUTSS and subindices are summarized for gender in table 2 and for age in table 3. Urgency There was a positive correlation between urgency and ADHD index when all patients with ADHD were evaluated (p 0.01, r 0.32, fig. 1, A). Further analyses regarding age revealed that urgency was Table 2. Total LUTSS and subindices by gender in patients with ADHD Males Females p Value Total LUTSS Nocturnal enuresis Constipation Urgency Holding maneuvers Voiding other symptoms Table 3. Total LUTSS and subindices by age in patients with ADHD 6 10 Yrs Yrs Yrs p Value Total LUTSS Nocturnal enuresis Constipation Urgency Holding maneuvers Voiding other symptoms positively correlated to ADHD index until age 13 years (for age 6 to 10 years p 0.017, r 0.38 and for age 10 to 13 years p 0.017, r 0.62; fig. 1, B and C). However, for age 13 to 17 years urgency was positively correlated with cognitive problems/inattention subscale score (p 0.009, r 0.77). When the combined effects of age and gender were analyzed, urgency was positively correlated with cognitive problems/inattention subscale score (p 0.045, r 0.71) and with ADHD index (p 0.008, r 0.84) in males 10 to 13 years old. There was also a positive correlation between urgency and cognitive problems/inattention subscale score in females 13 to 17 years old (p 0.01, r 0.87). Enuresis There was a positive correlation between enuresis in LUTSS and hyperactivity subscale score of CPRS-R when all patients with ADHD were evaluated (p 0.01, r 0.32, fig. 2, A). When patients with ADHD were analyzed by age, a positive correlation was observed between enuresis and hyperactivity subscale score only for patients 13 to 17 years old (p 0.01, r 0.88, fig. 2, B). Gender had no specific effect. Holding Maneuvers There was no correlation between holding maneuvers and any subscale scores of CPRS-R for patients with ADHD. Gender had no specific effect. For patients 6 to 10 years old holding maneuvers were positively correlated with ADHD index (p 0.036, r 0.34). Voiding and Other Symptoms There was no correlation between voiding and other symptoms and any subscale scores of CPRS-R for patients with ADHD. There was a positive correlation between voiding and other symptoms score and ADHD index in males 6 to 10 years old (p 0.046, r 0.48). Constipation Constipation subscore was not correlated to any subscale score of CPRS-R. Gender and age had no effect. DISCUSSION Although LUT problems are multifactorial and include organic and psychological factors, few studies

4 666 LOWER URINARY TRACT CONDITIONS IN CHILDREN WITH ATTENTION DEFICIT DISORDER Figure 1. A, positive correlation between urgency and ADHD index when all patients with ADHD were evaluated (p 0.01, r 0.32). B, positive correlation between urgency and ADHD index at age 6 to 10 years (p 0.017, r 0.38). C, positive correlation between urgency and ADHD index at age 10 to 13 years (p 0.017, r 0.62). have attempted to register both characteristics. Previous trials mostly demonstrated a significantly increased prevalence of ADHD in children with enuresis. 2 4,6 However, objective data evaluating the association between ADHD and various LUT dysfunctions have yet to be investigated. Although symptom scores cannot replace bladder diaries, they provide structured quantitative data to evaluate LUT dysfunction objectively. They offer an objective and scientific basis to grade symptoms for comparative research, as in our study. Although the necessity is controversial, the quantitative data provided for such studies are invaluable and more reliable. Whatever the cause, it is clear that a child diagnosed with ADHD should also be investigated for comorbid LUT problems and vice versa using objective diagnostic tools including validated questionnaires. Therefore, it is essential to explore whether there is any correlation between these questionnaires, which seem to be irrelevant to each other at first glance. Parallel to other reports, in our study frequency of daytime symptoms and enuresis, residual urine volume and pathological UFM rates were significantly higher in children diagnosed with ADHD than in controls. 3 5 The use of LUTSS in our series provides additional quantitative data regarding 5 main categories of voiding related symptomatology by investigating the possible correlations of enuresis, constipation, urgency, holding maneuvers, and voiding and other phase symptoms with ADHD. This quantitative questionnaire provides additional information in the literature, since previous studies have roughly categorized voiding problems as monosymptomatic and nonmonosymptomatic enuresis. Mean total LUTSS in the ADHD group was significantly higher than in controls. This score was also higher than the previously described cutoff value of 9 for defining the presence of bladder dysfunction in children using LUTSS. 15 This finding can either be explained by individuals who present with extremely high scores of LUTSS with severe voiding problems, or a general tendency of mild or moderate voiding problems among patients with ADHD. As shown in table 1, standard deviations and LUTSS range are low, which can serve as evidence for the increased frequency of voiding prob- Figure 2. A, positive correlation between nocturnal enuresis and hyperactivity subscale score when all patients with ADHD were evaluated (p 0.01, r 0.32). B, positive correlation between nocturnal enuresis and hyperactivity subscale score at age 13 to 17 years (p 0.01, r 0.88).

5 LOWER URINARY TRACT CONDITIONS IN CHILDREN WITH ATTENTION DEFICIT DISORDER 667 lems in children with ADHD. Also, the percentage of abnormal voiding diaries was significantly higher in the ADHD population (22%) than in controls (5%). In our series LUTSS subindices except the one evaluating constipation were significantly higher in patients with ADHD than in controls. These findings strongly underline that the incidence of LUT problems, not only enuresis, increases with ADHD. No significant difference was found in terms of the constipation related subindex of LUTSS. Since there is only 1 question regarding bowel status in the LUTSS, all children were also evaluated by BSS and no significant difference was noted. Quantitative evaluation of constipation provided us with additional support as coauthors of the LUTSS, due to our concerns regarding the capability of this scoring system to evaluate bowel status efficiently. 15 However, one should be aware that current definitions of constipation in the literature are poor guides to the presence or absence of bowel problems. No correlation was found between the total Conners and LUTSS scores in children with ADHD. Although statistically investigated for academic concern, the use of total CPRS-R is generally inapplicable clinically. ADHD index, cognitive problems/inattention, hyperactivity and oppositional subscale scores of this common checklist are generally used to provide data. We found positive correlations between total scores of CPRS-R and LUTSS, particularly for age (6 to 10 years) and gender (male). These findings are hard to interpret, since the use of total CPRS-R is clinically inapplicable and requires further investigation before widespread use. We observed striking results when subindex comparisons were performed. Initially all questioned symptoms in LUTSS were totally evaluated and mostly correlated with the ADHD index of the CPRS-R. Only enuresis was correlated with the hyperactivity subscale score. Constipation did not correlate with any subscale score of the CPRS-R for gender or age. If a child with ADHD has a high ADHD index per CPRS-R, he or she is more likely to have urgency. This correlation is most pronounced in boys 10 to 13 years old. If a child with ADHD has a high hyperactivity subscale score, he or she is more likely to have enuresis, which is more pronounced at ages 13 to 17 years. Although each case should be managed individually, this awareness can guide physicians dealing with ADHD to focus on specific voiding symptoms. Assessing CPRS-R and LUTSS and subindices of these questionnaires as part of a routine evaluation can determine the cooccurrence of both conditions. A legitimate question is, what is the clinical relevance of such correlations, and will they affect treatment strategy? For certain conditions urology outpatient clinics may be the first point of contact for a child with problems of emotion, attention and hyperactivity/impulsivity. Screening with such instruments may help to provide early detection of associated psychological problems. A major limitation of our study was that we focused on 1 aspect of this co-occurrence. We only investigated the presence of LUT dysfunction in children with ADHD and failed to evaluate children with bladder dysfunction for ADHD. However, a diagnosis of ADHD requires multimodal (diagnostic interview, questionnaires) and multiinformant (parents, teacher) assessment. 2 Investigating every child with dysfunctional voiding for ADHD would be difficult, while only evaluating mischievous, active children with voiding problems would generate a biased population. Additionally our hospital is a tertiary referral center and does not reflect the general incidence of ADHD among children with LUT dysfunction. Baeyens et al mentioned that children with enuresis referred to tertiary care may have a higher possibility of a comorbid ADHD diagnosis compared to children treated in nontertiary care. 2 Another limitation is the performance of UFM at strong urge, rather than when the child is comfortably full. We are aware that in children with normal bladder function the uroflow curve becomes progressively broader and the residual urine increases as the bladder becomes progressively overfull. We initially tried to perform uroflowmetry at comfortably full levels for both groups. However, the preliminary data revealed that the healthy controls at school and children with ADHD at the outpatient clinic claimed that they were full so that they could undergo the test and be finished as soon as possible, rather than waiting for their routine day-to-day sense of full. The majority of voided volumes were low. Therefore, despite knowing the disadvantages, to create a standard methodology we performed the tests at strong urge and repeated twice. For healthy controls our LUT dysfunction incidence is not higher than that in the literature. CONCLUSIONS Urgency and enuresis are the main voiding problems in children with ADHD. Simultaneous use of CPRS-R and LUTSS questionnaires should be encouraged in patients with ADHD to allow a structured and quantitative evaluation of these overlapping problems. Patients with ADHD demonstrating high scores in particular subscales of CPRS-R are more likely to have certain voiding symptoms. On this basis patients with both conditions could benefit from a multidisciplinary treatment approach.

6 668 LOWER URINARY TRACT CONDITIONS IN CHILDREN WITH ATTENTION DEFICIT DISORDER REFERENCES 1. Diagnostic and Statistical Manual of Mental Disorders, 4th ed, text revision (DSM-IV-TR). Arlington, Virginia: American Psychiatric Association Baeyens D, Roeyers H, D Haese L et al: The prevalence of ADHD in children with enuresis: comparison between a tertiary and non-tertiary care sample. Acta Paediatr 2006; 95: Baeyens D, Roeyers H, Erdeghem SV et al: The prevalence of attention deficit-hyperactivity disorder in children with nonmonosymptomatic nocturnal enuresis: a 4-year followup study. J Urol 2007; 178: Baeyens D, Roeyers H, Demeyere I et al: Attention-deficit/hyperactivity disorder (ADHD) as a risk factor for persistent nocturnal enuresis in children: a two-year follow-up study. Acta Paediatr 2005; 94: Baeyens D, Roeyers H, Walle JV et al: Behavioral problems and attention-deficit hyperactivity disorder in children with enuresis: a literature review. Eur J Pediatr 2005; 164: Robson WL, Jackson HP, Blackhurst D et al: Enuresis in children with attention-deficit hyperactivity disorder. South Med J 1997; 90: 503. EDITORIAL COMMENT 7. Biederman J, Santangelo SL, Faraone SV et al: Clinical correlates of enuresis in ADHD and non- ADHD children. J Child Psychol Psychiatry 1995; 36: Coghill D, Spiel G, Baldursson G et al: The ADORE study group. Which factors impact on clinician-rated impairment in children with ADHD? Eur Child Adolesc Psychiatry, suppl, 2006; 15: Hechtman L: Assessment and diagnosis of attention-deficit/hyperactivity disorder. Child Adolesc Psychiatr Clin N Am 2000; 9: Riley AW, Coghill D, Forrest CB et al: The ADORE study group. Validity of the health related quality of life assessment in the ADORE study: parent report form of the CHIP-CE edition. Eur Child Adolesc Psychiatry 2006; 15: Erhart M, Dopfner M, Sieberer UR and BELLA study group : Psychometric properties of two ADHD questionnaires: comparing the Conners scale and the FBB-HKS in the general population of German children and adolescents results of the BELLA study. Eur Child Adolesc Psychiatry, suppl, 2008; 17: Conners C: Symptom patterns in hyperkinetic, neurotic, and normal children. Child Dev 1970; 41: Conners CK, Sitarenios G, Parker JD et al: The revised Conners Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 1998; 26: Kaner S, Buyukozturk S, Iseri E et al: The validity and reliability study of the Turkish version of Conners Parent Rating Scale-revised (CPRS-R). In: Proceedings of 16th National Child and Adolescent Psychiatry Congress 2006; p Akbal C, Genc Y, Burgu B et al: Dysfunctional voiding and incontinence scoring system: quantitative evaluation of incontinence symptoms in pediatric population. J Urol 2005; 173: Kumar G and Steer RA: Factorial validity of the Conners Parent Rating Scale-revised: short form with psychiatric outpatients. J Pers Assess 2003; 80: Riegler G and Esposito I: Bristol scale stool form. A still valid help in medical practice and clinical research. Tech Coloproctol 2001; 5: 163. This study alerts the reader to the comorbidity between ADHD and LUT symptoms. What is new is that this is the first study to look systematically at a group of patients with ADHD. The authors conclude that voiding problems are more common in children with ADHD than in age matched controls. It seems of interest to look into the correlations within the ADHD group. Unfortunately the described correlations should be challenged. The observation that a child with a high hyperactivity score is more likely to have nocturnal symptoms, especially at ages 13 to 17 years, would not apply in daily practice. This observation could be the result of the low number of patients. Furthermore, what is the clinical relevance of finding correlations between specific domains of volume of distribution at steady state? Will we treat our patients differently? The authors refer to the task of doctors seeing patients with LUT symptoms to detect underlying ADHD using a simple tool. This is the relevant message. Piet Hoebeke Department of Urology and Pediatric Urology Ghent University Hospital Gent, Belgium