Journal of Pediatric Urology (2015) 11, 141.e1e141.e6
Incontinence in children with treated attention-deficit/hyperactivity disorder J. Niemczyk, M. Equit, L. Hoffmann, A. von Gontard Summary Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany Correspondence to: J. Niemczyk, Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany, Tel.: þ49 6841 16 24385; fax: þ49 6841 16 24397 [email protected] (J. Niemczyk) Keywords Attention-deficit/hyperactivity disorder; Functional incontinence; Enuresis; Daytime urinary incontinence; Fecal incontinence; Delayed bladder and bowel control Received 8 October 2014 Accepted 24 February 2015 Available online 12 March 2015
Introduction Attention-deficit/hyperactivity disorder (ADHD) and incontinence (nocturnal enuresis, daytime urinary incontinence and fecal incontinence) are common disorders in childhood. Both disorders are strongly associated with each other. Objective ADHD can affect compliance to incontinence therapy in a negative way; it can also affect outcome. The aim of the present study was to assess the prevalence of incontinence, age of bladder and bowel control, and psychological symptoms in children having treatment for ADHD compared to a control group. Study design Forty children having treatment for ADHD (75% boys, mean age 11.4 years) and 43 matched controls (60.5% boys, mean age 10.7 years) were assessed. Their parents filled out questionnaires to assess: child psychopathology (Child Behavior Checklist), incontinence (Parental Questionnaire: Enuresis/Urinary Incontinence; Encopresis Questionnaire e Screening Version) and symptoms of the lower urinary tract (International-Consultation-on-Incontinence-Questionnaire e Pediatric Lower Urinary Tract Symptoms). The ICD-10 diagnoses and children’s IQ were measured by standardized instruments (Kinder-DIPS, Coloured Progressive Matrices/Standard Progressive Matrices).
Results Rates of incontinence in the ADHD group (5% nocturnal enuresis, 5% daytime urinary incontinence, 2.5% fecal incontinence) did not differ significantly from incontinence rates in the control group (4.7% daytime urinary incontinence). More children in the ADHD group had Child Behavior Checklist scores in the clinical range. Further ICD-10 disorders were present in eight children with ADHD and in one control child. More children with ADHD had delayed daytime and nighttime bladder control, as well as delayed bowel control, than the controls. Discussion The present study showed that if children are treated for their ADHD, according to standard practice guidelines, incontinence rates are similar to those without ADHD. More children with ADHD reached continence at a later age than the controls, which could be an indicator of maturational deficits in the central nervous system. Additionally, children with ADHD showed higher rates of clinically relevant psychological symptoms. Conclusion This study provides further information of the association between ADHD and incontinence. Treatment of ADHD may be associated with positive effects on incontinence outcomes. Therefore, children with ADHD should always be screened for incontinence problems and children with incontinence problems should also be screened for ADHD if symptoms of hyperactivity, inattention and/or impulsivity are also present.
Rates of incontinence and psychological symptoms in children with attention-deficit/hyperactivity disorder and the controls ADHD group (n Z 40) Subtypes of incontinence Any incontinence n (%) NE n (%) DUI n (%) FI n (%) Clinically relevant CBCL scores CBCL total score >90th percentile n (%) CBCL Externalizing score >90th percentile n (%) CBCL Internalizing score >90th percentile n (%)
4 2 2 1
Control group (n Z 43)
(10.0) (5.0) (5.0) (2.5)
2 (4.7) e 2 (4.7) e
23 (57.5) 19 (47.5) 16 (40.0)
1 (2.3) e 4 (9.3)
ADHD, Attention-deficit/hyperactivity disorder; CBCL, Child Behavior Checklist; DUI, daytime urinary incontinence; FI, fecal incontinence; NE, nocturnal enuresis. http://dx.doi.org/10.1016/j.jpurol.2015.02.009 1477-5131/ª 2015 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
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J. Niemczyk et al.
Introduction
Material and methods
Attention-Deficit/Hyperactivity Disorder (ADHD) is defined as a persistent pattern of inattention, hyperactivity and/or impulsivity that causes impairment, with an onset before the age of 12 [1,2]. It is present in about 5% of children, with a higher risk for boys [2]. Three different presentations are diagnosable: predominantly inattentive, predominantly hyperactive/impulsive, and combined [2]. The etiology is multifactorial, with a high genetic component; environmental, social and biological factors also play a major role [3]. Functional incontinence such as nocturnal enuresis (NE), daytime urinary incontinence (DUI) and fecal incontinence (FI) are common in childhood. Nocturnal enuresis is diagnosed as intermittent leakage of urine during sleep in children older than 5 years, with at least one episode per month after excluding organic causes [2,4,5]. Daytime urinary incontinence is defined as wetting during the day in combination with lower urinary tract symptoms (LUTS) [4]. The terms fecal incontinence and encopresis are used synonymously; both describe defecation into inappropriate places in children older than 4 years, with at least one episode per month after ruling out organic factors [2]. Prevalence in 7-year-old children is about 10% for NE, 3% for DUI and 1e3% for FI [6]. Prevalence of ADHD is higher in children with incontinence than in continent children. In a population-based study, parents described attention and activity problems in 17.6% of bedwetting and in 24.8% of daytime wetting children [7,8]. In FI, rates of ADHD are 9.2% for children with frequent soiling (1 x/week or more) [9]; vice versa, rates of incontinence are higher in children with ADHD. Most studies have focused on NE, with a prevalence of 20.9e28.6% of NE in children with ADHD [10e12]. Fewer studies have addressed DUI and FI. In one study, DUI was 6.5% in 6-year-old children and 13.1% in 6e14-year-old children [11]. In another study, children with ADHD had higher rates of lower urinary tract symptoms (LUTS) compared to the controls [13]. In a population-based study, the rate of FI in ADHD was 4.1% [14]. All mentioned studies indicate a special association of incontinence and ADHD, with higher co-occurrence than expected by chance, which is described in detail in a recent review [15]. However, common etiological factors between incontinence and ADHD have not been clarified in detail. Genetic factors are important for NE and ADHD alone, but there is no evidence for a common genetic transmission of both disorders together [16]. Maturational deficits of the central nervous system are a possible shared etiological factor. Further studies have shown that children with ADHD are less compliant to treatment of incontinence and have a less favorable therapy outcome, especially if this requires cooperation [17e19]. On the other hand, in anecdotal case reports, incontinence dissolved after treating ADHD with stimulants [20]. As previous literature has shown associations between ADHD, therapy of ADHD and incontinence, the aims of the present study were to assess the prevalence of incontinence, age of bladder and bowel control, and psychological symptoms in children with treated ADHD compared to a control group.
All consecutively treated children with ADHD who were referred to a tertiary outpatient department of child and adolescent psychiatry over a period of 3 months (AprileJune 2013) were recruited. Children who were presented for the first time and received a diagnosis of ADHD, as well as children with confirmed ADHD who were presented for follow-up, were included. Children with severe medical conditions or intellectual disability (IQ < 70) were excluded (n Z 3). The remaining ADHD group consisted of 30 boys (75%) and 10 girls, with a mean age of 11.4 years (SD 2.49 years, range 7e17 years). A total of 28 children were diagnosed with the inattentional subtype (70%), four with the hyperactive/ impulsive (10%) subtype and eight with the combined subtype (20%) according to the criteria of the Diagnostic and Statistical Manual of Mental Disorders e Fourth Edition (DSM-IV). All children were treated by a multimodal approach according to evidence-based guidelines consisting of psychoeducation, behavioral therapy (including parental training, positive reinforcement) and additional pharmacotherapy, if needed. A total of 77.5% of the ADHD group were treated with stimulants (methylphenidate) and one child was treated with atomoxetine. A healthy control group of 43 children, who were matched regarding gender and age (60.5% male, mean age 10.7 years, SD 3.03 years, range 5e17 years), was recruited from sports clubs or schools. The groups did not differ significantly in age or gender distribution. Children of the ADHD group received standard psychological and physical examination in the outpatient clinic. Children of both groups were assessed in the 3-month study interval. A structured diagnostic interview to assess comorbid psychiatric disorders in children (“Diagnostisches Interview bei psychischen Sto ¨rungen von Kindern und Jugendlichen” Z Kinder-DIPS) [21] was conducted with parents of both groups. Parents were also asked to fill out the Child Behavior Checklist (CBCL) [22] to assess child psychopathology, the Parental Questionnaire: Enuresis/ Urinary Incontinence and Encopresis Questionnaire e Screening Version [23,24] and the German version of the International-Consultation-on-Incontinence-Questionnaire e Pediatric Lower Urinary Tract Symptoms (ICIQ-CLUTS) [25]. Additionally, IQ was measured in all children by a onedimensional intelligence test (Coloured Progressive Matrices (CPM) or Standard Progressive Matrices (SPM)) [26,27]. Nocturnal enuresis and DUI were diagnosed according to the International Children’s Continence Society (ICCS) criteria [4] (i.e. from the age of 5 years onwards when wetting occurs at least once per month). Fecal incontinence was diagnosed from the age of 4 years if soiling occurred at least once per month, according to DSM-5 criteria [2]. A mean LUTS score >13 in the ICIQ-CLUTS was considered to be clinically relevant. Delayed bladder control was defined by reaching urinary continence at an age of 5 years or older. Delayed bowel control was defined in children reaching bowel continence at 4 years of age or older. The CBCL total, internalizing and externalizing scale were regarded as clinically relevant with a T-value >63 (90th percentile). Statistical analyses were conducted with IBM SPSS Statistics for Windows, Version 22.0 (IBM Corp., Armonk, NY;
Incontinence in children
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Table 1 Descriptive data: gender, age, IQ, behavioral symptoms, psychological disorders (DSM-5) and incontinence in children with attention-deficit/hyperactivity disorder and the controls. Boys n (%) Girls n (%) Mean age in years (SD) Mean IQ (SD) Mean CBCL total T-value (SD) Mean CBCL Ext T-value (SD) Mean CBCL Int T-value (SD) CBCL total score >90th percentile n (%) CBCL Ext score >90th percentile n (%) CBCL Int score >90th percentile n (%) Psychiatric diagnoses Internalizing disordersc n (%) Externalizing disordersd n (%) Incontinence overallb n (%) NE n (%) DUI n (%) FI n (%) Mean LUTS score (SD)
ADHD group (n Z 40)
Control group (n Z 43)
Significancea
30 10 11.4 101.3 65.1 63.6 60.0 23 19 16
(75.0) (25.0) (2.49) (18.66) (8.51) (9.21) (8.49) (57.5) (47.5) (40.0)
26 17 10.7 110.9 47.4 46.1 50.4 1 e 4
n.s.
(10.0) (10.0) (10.0) (5.0) (5.0) (2.5) (1.67)
e
4 4 4 2 2 1 4.3
(60.5) (39.5) (3.03) (15.77) (10.60) (8.46) (9.88) (2.3) (9.3)
1 (2.3) 2 (4.7) e 2 (4.7) e 3.9 (1.52)
n.s. p Z 0.013* p < 0.001* p < 0.001* p < 0.001* p < 0.001* p < 0.001* p Z 0.001*
n.s. n.s. n.s. n.s. n.s.
ADHD Z attention-deficit/hyperactivity disorder; CBCL Z child behavior checklist; CBCL Ext Z CBCL externalizing; CBCL Int Z CBCL internalizing; DUI Z daytime urinary incontinence; FI Z fecal incontinence; NE Z nocturnal enuresis. *Statistical significance at a statistical level of at least p < .05. Bold Z statistically significant result; Italics Z Student t-tests conducted. a Chi-squared test for non-parametric data and t-test for parametric variables. b At least one subtype of incontinence. c Generalized anxiety disorder, specific phobia, separation anxiety disorder. d Conduct disorder, oppositional defiant disorder.
2013), using descriptive statistics, nonparametric (Chisquaredetests, Fisher’s Exact tests) and parametric tests (ttests). Results were considered to be significant at a p-value of 0.05. The local ethics committee approved the study.
Results Descriptive data, incontinence rates, CBCL scores and child psychiatric diagnoses for both groups are shown in Table 1: 10% of the ADHD group were affected by incontinence; two children had NE; one had DUI; and one child had both DUI and FI. Incontinence rates in the control group did not differ significantly: only two children were affected by DUI and none had NE or FI. No significant differences were found regarding the mean LUTS score between the ADHD and control groups (4.3 vs 3.9). No children reached the clinically relevant score of 13. Children with ADHD had a significantly lower IQ (101 vs 111) than the controls (Table 1). Compared to the controls,
Table 2
the ADHD group had significantly more clinically relevant scores in the CBCL total (57.5% vs 2.3%), externalizing and internalizing scale (Table 1). Eight children of the ADHD group (20%) and one control child (2.3%) were diagnosed with a comorbid psychological disorder. Diagnoses in the ADHD group were specific phobia, generalized anxiety disorder, separation anxiety disorder, conduct disorder and oppositional defiant disorder. The control child had oppositional defiant disorder. Incontinence was present in one child with ADHD and a comorbid disorder, but not in the control child with comorbidity. Information on bladder and bowel control is shown in Table 2. Children in the ADHD group reached bladder and bowel control at a mean age of 3.05 years (SD 1.45) during the day, and 3.97 years (SD 2.59) during the night. Children in the control group reached bladder control at a mean age of 2.64 years (SD 0.49) during the day and 3.24 years (SD 0.94) during the night. Bowel control was achieved at a mean age of 2.95 years (SD 1.53) in the ADHD and 2.66 years (SD 0.5) in the control group. The mean ages were slightly
Delayed bladder and bowel control in children with attention-deficit/hyperactivity disorder and the controls.
Delayed daytime bladder control (>5 years) n (%) Delayed nighttime bladder control (>5 years) n (%) Delayed bowel control (>4 years) n (%)
ADHD group (n Z 40)
Control group (n Z 43)
Significance
6 (15.8) 10 (27.0) 9 (27.3)
e 4 (9.3) 3 (7.1)
p Z 0.009*,a p Z 0.037* p Z 0.018*
ADHD, attention-deficit/hyperactivity disorder. *Statistical significance at a statistical level of at least p < .05. a Fisher’s Exact test.
141.e4 higher in the ADHD group, but did not reach statistical significance. However, significantly more children with ADHD had delayed daytime and nighttime bladder control, as well as delayed bowel control, than children in the control group (Table 2). Comparing the inattentive subtype (70%) to the hyperactive/impulsive (10%) and combined subtypes (20%) within the ADHD group, no significant differences were found regarding: incontinence (10.7 vs 8.3%, Fishers Exact test, p Z 1.0); delayed nighttime bladder control (32.0 vs 16.7%, Fishers Exact test, p Z 0.45); daytime bladder control (19.2 vs 8.3%, Fishers Exact test, p Z 0.64); and bowel control (28.6 vs 25.0%; Fishers Exact test, p Z 1.0).
Discussion This is one of the first studies examining incontinence in children who have already received treatment for ADHD. The results indicate that children with an optimal, guideline-oriented treatment of ADHD show no higher rates of incontinence than children without ADHD. In contrast to other findings, incontinence rates in ADHD children in the present study were much lower (NE 5%, DUI 5% and FI 2.5%) than in former studies, especially for NE. One explanation for these low incontinence rates could be that the majority of the ADHD group was already treated with stimulants. This could have had a positive effect on incontinence, as has previously been shown [20]. On the other hand, medication could have improved compliance in the incontinence treatment. In addition, children in the present study received a full child psychiatric assessment, counseling and cognitive-behavioral interventions for ADHD according to evidence-based guidelines. This could also have contributed towards the low rates. However, in this study, incontinence rates at the beginning of ADHD treatment were not assessed. Only longitudinal studies can clarify how far medical treatment with stimulants can affect therapy outcomes of incontinence in children with ADHD. Another explanation for this discrepancy could be the older age of participants. In most of the cited studies, children were younger than in the present study (6e8.7 years vs 11.4 years) [10e12]. Both NE and DUI have spontaneous cure rates e for NE this is up to 15% per year [6]. Older children with ADHD, as examined in the present study, were affected by incontinence in their younger years (up to 27.3% with delayed bladder/bowel control), which had resolved. This explanation is partially supported by Robson et al., who found a significant difference between children with ADHD and controls regarding retrospective NE rates at the age of 6 years, but no difference at the children’s current age (mean 11.2 years) [11]. In that study, NE rates of 3.9% in older children were comparable with those in the present study, whereas DUI rates were still high (13.1%). Only a few studies have assessed the effects of delayed bladder and bowel control in children with ADHD. Although the mean ages of bladder and bowel control did not differ between the groups, the greater standard deviations in the ADHD group indicate a larger variability in reaching continence. Children with ADHD are a more heterogeneous group regarding bladder and bowel control, indicating that
J. Niemczyk et al. subgroups of ADHD patients could be affected by developmental delays and incontinence. In a longitudinal study, children with persisting NE after the age of 10 years had significantly higher risks for attention-deficit, conduct problems and anxiety throughout adolescence than those who achieved continence before the age of 5 years [28]. The greater number of children with delayed bladder and bowel control in the ADHD group could be an indicator for maturational deficits as a common association in incontinence and ADHD. To confirm these findings, age of reaching bladder and bowel control should be assessed in a prospective design. In NE, maturational deficits of the brainstem are assumed, which are supported by findings of arousal deficits and a decreased prepulse inhibition [15]. Additionally, children with NE show a slower motor performance, suggesting maturational deficits in other cortical areas too [29]. Children with ADHD can have deficits in their cognitive processes, attention and motor planning [30] and are also at higher risk of developmental delays (e.g. in motor and speech development and achieving continence) [10]. However, children with ADHD with NE were not more incapacitated than children with ADHD without NE [15]. Research on etiological factors of the association between ADHD and DUI or FI is lacking. Other studies have found that NE is associated more with inattentive than with hyperactive/impulsive ADHD symptoms [16]. In the present study, the majority of the ADHD participants had the inattentive subtype, followed by the combined and hyperactive/impulsive subtype. In population-based samples, most of the ADHD children have the combined subtype (w60%), which is different to the present study [31]. The inattentive subtype is the most difficult to diagnose, as other disorders have to be excluded. The ADHD subtypes were diagnosed by: a full psychiatric assessment, a structured interview, an IQ-test and questionnaires. Despite this detailed assessment, no significant differences between the subtypes could be found, but this could also be explained by the small sample sizes. The present study confirmed that children with ADHD have a high risk for additional behavioral problems. The higher CBCL total, externalizing and internalizing rates in the ADHD group show that these children are not only impaired by attentional, hyperactive and impulsive problems, but also by a variety of additional comorbid psychological problems. These can negatively affect incontinence therapy, outcome and compliance as well. Regarding pharmacological treatment, compliance and outcome rates did not differ between the ADHD children and controls [17]. In NE and/or DUI, drug therapy for incontinence shows satisfactory outcomes in children with ADHD, but lower cure rates than in children without ADHD [18]. In FI, children with ADHD are also at higher risk for a worse treatment outcome [19]. On the other hand, treatment of ADHD, especially medication, can improve treatment outcome of incontinence. As methylphenidate does not seem to have an antienuretic effect, Williamson et al. speculated that stimulants may decrease the sleep arousal threshold and lead to awakening of the child before wetting [20]. The present study shows that in a highly impaired subgroup of children with treated ADHD, incontinence rates
Incontinence in children are relatively low at an older age. Although many of these children reach bladder and bowel control later in life, these problems do not necessarily persist. As evidence-based therapy options are available for both incontinence and ADHD [3,23,24], both should be offered. This underlines the importance of diagnosing both incontinence and comorbid disorders. All children with ADHD should be screened for incontinence when presented in a healthcare setting, just as vice versa, children with incontinence should be screened for comorbid disorders.
Strengths and limitations A major strength of the study was the design including a healthy, matched control group from the community and not a convenience sample. Also, all children were included who presented consecutively at a tertiary care center. All children with ADHD had been diagnosed by both a mentalhealthcare expert and by a structured, standardized diagnostic interview. All children treated for ADHD received a multimodal approach of treatment including behavioral therapy and pharmacotherapy. This study provides first data on the association between treated ADHD, incontinence and bladder/bowel control in psychiatrically treated children compared to controls. A limitation was the heterogeneous group of older ADHD patients differing in subtypes and treatment. Children in the ADHD group also differed in treatment duration for ADHD, and incontinence rates at the beginning of ADHD treatment were not known. Type and duration of ADHD and incontinence treatment were not assessed systematically. The sample was recruited from a tertiary outpatient clinic, which can lead to selection biases. Another limitation was that incontinence was only assessed by parental questionnaires and not by a 48-h voiding diary, uroflowmetry and sonography, which should be considered in future studies. In future studies, the effect and type of ADHD treatment on incontinence rates (before and after ADHD treatment) should be examined in more detail.
Conclusion This study provides further information of the association between ADHD and incontinence. Children with ADHD are not only impaired by problems of attention, hyperactivity and impulsivity, but also by delayed bladder and bowel control. However, in children who are treated for their ADHD according to standard guidelines, incontinence rates are not higher than in children without ADHD. Children with ADHD should be screened for incontinence e and children with incontinence should be screened for ADHD e if symptoms of inattention, hyperactivity or impulsivity are present.
Conflict of interest statement Nil.
Funding Nil.
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Ethical approval The study was approved by the local ethics committee.
References [1] American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorders, text revision (DSM-IV-TR). Washington, D.C.: American Psychiatric Association; 2000. [2] American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorders e Fifth Edition (DSM 5). Washington, D.C.: APA; 2013. [3] Moriyama TS, Cho AJM, Verin RE, Fuentes J, Polanczyk GV. Attention deficit hyperactivity disorder. In: Rey JM, editor. IACAPAP e-Textbook of Child and Adolescent Mental Health. Geneva: International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http:// iacapap.org/wp-content/uploads/D.1-ADHD-072012.pdf [last accessed 08 October 2014]. [4] Austin PF, Bauer SB, Bower W, Chase J, Franco I, Hoebeke P, et al. The standardization of terminology of lower urinary tract function in children and adolescents: update report from the Standardization Committee of the International Children’s Continence Society. J Urol 2014;191:1863e5. [5] World Health Organization (WHO). The ICD-10 classification of mental and behavioural disorders e diagnostic criteria for research. Geneva: WHO; 1993. [6] Von Gontard A, Neve ´us T. Management of bladder and bowel control in children. London: MacKeith Press; 2006. [7] Joinson C, Heron J, Emond A, Butler R. Psychological problems in children with bedwetting and combined (day and night) wetting: a UK population-based study. J Pediatr Psychol 2007; 32:605e16. [8] Joinson C, Heron J, Von Gontard A. Psychological problems in children with daytime wetting. Pediatrics 2006;118: 1985e93. [9] Joinson C, Heron J, Butler U, Von Gontard A. Psychological differences between children with and without soiling problems. Pediatrics 2006;117:1575e84. [10] Bhatia MS, Nigam VR, Bohra N, Malik SC. Attention deficit disorder with hyperactivity among paediatric outpatients. J Child Psychol Psychiatry Allied Discip 1991;32:297e306. [11] Robson WLM, Jackson HP, Blackhurst D, Leung AKC. Enuresis in children with attention-deficit hyperactivity disorder. South Med J 1997;90:503e5. [12] Yang T, Huang K, Chen S, Chang H, Yang H, Guo Y. Correlation between clinical manifestations of nocturnal enuresis and attentional performance in children with attention deficit hyperactivity disorder (ADHD). J Formos Med Assoc 2013;112: 41e7. [13] Duel BP, Steinberg-Epstein R, Hill M, Lerner M, Koff S, De Gennaro M, et al. A survey of voiding dysfunction in children with attention deficit-hyperactivity disorder. J Urol 2003;170: 1521e4. [14] Mckeown C, Hisle-Gorman E, Eide M, Gorman GH, Nylund CM. Association of constipation and fecal incontinence with attention-deficit/hyperactivity disorder. Pediatrics 2013;132: e1210e5. [15] von Gontard A, Equit M. Comorbidity of ADHD and incontinence in children. Eur Child Adolesc Psychiatry 2015;24: 127e40. [16] Elia J, Takeda T, Deberardinis R, Burke J, Accardo J, Ambrosini PJ, et al. Nocturnal enuresis: a suggestive endophenotype marker for a subgroup of inattentive attention-deficit/hyperactivity disorder. J Pediatr 2009;155: 239e44.
141.e6 [17] Crimmins CR, Rathbun SR, Husmann DA. Management of urinary incontinence and nocturnal enuresis in attention-deficit hyperactivity disorder. J Urol 2003;170:1347e50. [18] Gor RA, Fuhrer J, Schober JM. A retrospective observational study of enuresis, daytime voiding symptoms, and response to medical therapy in children with attention deficit hyperactivity disorder and autism spectrum disorder. J Pediatr Urol 2012;8:314e7. [19] Van Everdingen-Faasen EQ, Gerritsen BJ, Mulder PGH, Fliers EA, Groeneweg M. Psychosocial co-morbidity affects treatment outcome in children with fecal incontinence. Eur J Pediatr 2008;167:985e9. [20] Williamson LB, Gower M, Ulzen T. Enuresis and ADHD in older children and an adolescent treated with stimulant medication: a case series. J Can Acad Child Adolesc Psychiatry 2011; 20:53e5. [21] Schneider S, Margraf J, Unnewehr S. Kinder-DIPS: Diagnostisches Interview bei psychischen Sto ¨rungen von Kindern und Jugendlichen. Berlin: Springer; 1995. [22] Achenbach TM. Manual for the child behavior checklist/4-18 and 1991 profile. Burlington, VT: University of Vermont; 1991. [23] Von Gontard A. Enuresis. In: Rey JM, editor. IACAPAP e-Textbook of Child and Adolescent Mental Health. Geneva: International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http://iacapap.org/wpcontent/uploads/C.4-ENURESIS-072012.pdf [last accessed 08 October 2014]. [24] Von Gontard A. Encopresis. In: Rey JM, editor. IACAPAP eTextbook of Child and Adolescent Mental Health. Geneva:
J. Niemczyk et al.
[25]
[26]
[27] [28]
[29]
[30]
[31]
International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http://iacapap.org/wpcontent/uploads/C.5-ENCOPRESIS-0072012.pdf [last accessed 08 October 2014]. De Gennaro M, Niero M, Capitanucci ML, Von Gontard A, Woodward M, Tubaro A, et al. Validity of the international consultation on incontinence questionnaire-pediatric lower urinary tract symptoms: a screening questionnaire for children. J Urol 2010;184:1662e7. Raven J, Raven JC, Court JH. Raven’s progressive matrices und vocabulary scales. Frankfurt: Harcourt Test Services; 2006. Raven JC. Standard progressive matrices. Go ¨ttingen: BeltzTest; 1998. Fergusson DM, Horwood LJ. Nocturnal enuresis and behavioral problems in adolescence: a 15-year longitudinal study. Pediatrics 1994;94:662e8. von Gontard A, Freitag CM, Seifen S, Pukrop R, Ro ¨hling D. Neuromotor development in nocturnal enuresis. Dev Med Child Neurol 2006;48:744e50. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A 2007;104:19649e54. Elia J, Arcos-Burgos M, Bolton KL, Ambrosini PJ, Berrettini W, Muenke M. ADHD latent class clusters: DSM-IV subtypes and comorbidity. Psychiatry Res 2009;170:192e8.
Incontinence in children with treated attention-deficit/hyperactivity disorder J. Niemczyk, M. Equit, L. Hoffmann, A. von Gontard Summary Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany Correspondence to: J. Niemczyk, Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany, Tel.: þ49 6841 16 24385; fax: þ49 6841 16 24397 [email protected] (J. Niemczyk) Keywords Attention-deficit/hyperactivity disorder; Functional incontinence; Enuresis; Daytime urinary incontinence; Fecal incontinence; Delayed bladder and bowel control Received 8 October 2014 Accepted 24 February 2015 Available online 12 March 2015
Introduction Attention-deficit/hyperactivity disorder (ADHD) and incontinence (nocturnal enuresis, daytime urinary incontinence and fecal incontinence) are common disorders in childhood. Both disorders are strongly associated with each other. Objective ADHD can affect compliance to incontinence therapy in a negative way; it can also affect outcome. The aim of the present study was to assess the prevalence of incontinence, age of bladder and bowel control, and psychological symptoms in children having treatment for ADHD compared to a control group. Study design Forty children having treatment for ADHD (75% boys, mean age 11.4 years) and 43 matched controls (60.5% boys, mean age 10.7 years) were assessed. Their parents filled out questionnaires to assess: child psychopathology (Child Behavior Checklist), incontinence (Parental Questionnaire: Enuresis/Urinary Incontinence; Encopresis Questionnaire e Screening Version) and symptoms of the lower urinary tract (International-Consultation-on-Incontinence-Questionnaire e Pediatric Lower Urinary Tract Symptoms). The ICD-10 diagnoses and children’s IQ were measured by standardized instruments (Kinder-DIPS, Coloured Progressive Matrices/Standard Progressive Matrices).
Results Rates of incontinence in the ADHD group (5% nocturnal enuresis, 5% daytime urinary incontinence, 2.5% fecal incontinence) did not differ significantly from incontinence rates in the control group (4.7% daytime urinary incontinence). More children in the ADHD group had Child Behavior Checklist scores in the clinical range. Further ICD-10 disorders were present in eight children with ADHD and in one control child. More children with ADHD had delayed daytime and nighttime bladder control, as well as delayed bowel control, than the controls. Discussion The present study showed that if children are treated for their ADHD, according to standard practice guidelines, incontinence rates are similar to those without ADHD. More children with ADHD reached continence at a later age than the controls, which could be an indicator of maturational deficits in the central nervous system. Additionally, children with ADHD showed higher rates of clinically relevant psychological symptoms. Conclusion This study provides further information of the association between ADHD and incontinence. Treatment of ADHD may be associated with positive effects on incontinence outcomes. Therefore, children with ADHD should always be screened for incontinence problems and children with incontinence problems should also be screened for ADHD if symptoms of hyperactivity, inattention and/or impulsivity are also present.
Rates of incontinence and psychological symptoms in children with attention-deficit/hyperactivity disorder and the controls ADHD group (n Z 40) Subtypes of incontinence Any incontinence n (%) NE n (%) DUI n (%) FI n (%) Clinically relevant CBCL scores CBCL total score >90th percentile n (%) CBCL Externalizing score >90th percentile n (%) CBCL Internalizing score >90th percentile n (%)
4 2 2 1
Control group (n Z 43)
(10.0) (5.0) (5.0) (2.5)
2 (4.7) e 2 (4.7) e
23 (57.5) 19 (47.5) 16 (40.0)
1 (2.3) e 4 (9.3)
ADHD, Attention-deficit/hyperactivity disorder; CBCL, Child Behavior Checklist; DUI, daytime urinary incontinence; FI, fecal incontinence; NE, nocturnal enuresis. http://dx.doi.org/10.1016/j.jpurol.2015.02.009 1477-5131/ª 2015 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
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J. Niemczyk et al.
Introduction
Material and methods
Attention-Deficit/Hyperactivity Disorder (ADHD) is defined as a persistent pattern of inattention, hyperactivity and/or impulsivity that causes impairment, with an onset before the age of 12 [1,2]. It is present in about 5% of children, with a higher risk for boys [2]. Three different presentations are diagnosable: predominantly inattentive, predominantly hyperactive/impulsive, and combined [2]. The etiology is multifactorial, with a high genetic component; environmental, social and biological factors also play a major role [3]. Functional incontinence such as nocturnal enuresis (NE), daytime urinary incontinence (DUI) and fecal incontinence (FI) are common in childhood. Nocturnal enuresis is diagnosed as intermittent leakage of urine during sleep in children older than 5 years, with at least one episode per month after excluding organic causes [2,4,5]. Daytime urinary incontinence is defined as wetting during the day in combination with lower urinary tract symptoms (LUTS) [4]. The terms fecal incontinence and encopresis are used synonymously; both describe defecation into inappropriate places in children older than 4 years, with at least one episode per month after ruling out organic factors [2]. Prevalence in 7-year-old children is about 10% for NE, 3% for DUI and 1e3% for FI [6]. Prevalence of ADHD is higher in children with incontinence than in continent children. In a population-based study, parents described attention and activity problems in 17.6% of bedwetting and in 24.8% of daytime wetting children [7,8]. In FI, rates of ADHD are 9.2% for children with frequent soiling (1 x/week or more) [9]; vice versa, rates of incontinence are higher in children with ADHD. Most studies have focused on NE, with a prevalence of 20.9e28.6% of NE in children with ADHD [10e12]. Fewer studies have addressed DUI and FI. In one study, DUI was 6.5% in 6-year-old children and 13.1% in 6e14-year-old children [11]. In another study, children with ADHD had higher rates of lower urinary tract symptoms (LUTS) compared to the controls [13]. In a population-based study, the rate of FI in ADHD was 4.1% [14]. All mentioned studies indicate a special association of incontinence and ADHD, with higher co-occurrence than expected by chance, which is described in detail in a recent review [15]. However, common etiological factors between incontinence and ADHD have not been clarified in detail. Genetic factors are important for NE and ADHD alone, but there is no evidence for a common genetic transmission of both disorders together [16]. Maturational deficits of the central nervous system are a possible shared etiological factor. Further studies have shown that children with ADHD are less compliant to treatment of incontinence and have a less favorable therapy outcome, especially if this requires cooperation [17e19]. On the other hand, in anecdotal case reports, incontinence dissolved after treating ADHD with stimulants [20]. As previous literature has shown associations between ADHD, therapy of ADHD and incontinence, the aims of the present study were to assess the prevalence of incontinence, age of bladder and bowel control, and psychological symptoms in children with treated ADHD compared to a control group.
All consecutively treated children with ADHD who were referred to a tertiary outpatient department of child and adolescent psychiatry over a period of 3 months (AprileJune 2013) were recruited. Children who were presented for the first time and received a diagnosis of ADHD, as well as children with confirmed ADHD who were presented for follow-up, were included. Children with severe medical conditions or intellectual disability (IQ < 70) were excluded (n Z 3). The remaining ADHD group consisted of 30 boys (75%) and 10 girls, with a mean age of 11.4 years (SD 2.49 years, range 7e17 years). A total of 28 children were diagnosed with the inattentional subtype (70%), four with the hyperactive/ impulsive (10%) subtype and eight with the combined subtype (20%) according to the criteria of the Diagnostic and Statistical Manual of Mental Disorders e Fourth Edition (DSM-IV). All children were treated by a multimodal approach according to evidence-based guidelines consisting of psychoeducation, behavioral therapy (including parental training, positive reinforcement) and additional pharmacotherapy, if needed. A total of 77.5% of the ADHD group were treated with stimulants (methylphenidate) and one child was treated with atomoxetine. A healthy control group of 43 children, who were matched regarding gender and age (60.5% male, mean age 10.7 years, SD 3.03 years, range 5e17 years), was recruited from sports clubs or schools. The groups did not differ significantly in age or gender distribution. Children of the ADHD group received standard psychological and physical examination in the outpatient clinic. Children of both groups were assessed in the 3-month study interval. A structured diagnostic interview to assess comorbid psychiatric disorders in children (“Diagnostisches Interview bei psychischen Sto ¨rungen von Kindern und Jugendlichen” Z Kinder-DIPS) [21] was conducted with parents of both groups. Parents were also asked to fill out the Child Behavior Checklist (CBCL) [22] to assess child psychopathology, the Parental Questionnaire: Enuresis/ Urinary Incontinence and Encopresis Questionnaire e Screening Version [23,24] and the German version of the International-Consultation-on-Incontinence-Questionnaire e Pediatric Lower Urinary Tract Symptoms (ICIQ-CLUTS) [25]. Additionally, IQ was measured in all children by a onedimensional intelligence test (Coloured Progressive Matrices (CPM) or Standard Progressive Matrices (SPM)) [26,27]. Nocturnal enuresis and DUI were diagnosed according to the International Children’s Continence Society (ICCS) criteria [4] (i.e. from the age of 5 years onwards when wetting occurs at least once per month). Fecal incontinence was diagnosed from the age of 4 years if soiling occurred at least once per month, according to DSM-5 criteria [2]. A mean LUTS score >13 in the ICIQ-CLUTS was considered to be clinically relevant. Delayed bladder control was defined by reaching urinary continence at an age of 5 years or older. Delayed bowel control was defined in children reaching bowel continence at 4 years of age or older. The CBCL total, internalizing and externalizing scale were regarded as clinically relevant with a T-value >63 (90th percentile). Statistical analyses were conducted with IBM SPSS Statistics for Windows, Version 22.0 (IBM Corp., Armonk, NY;
Incontinence in children
141.e3
Table 1 Descriptive data: gender, age, IQ, behavioral symptoms, psychological disorders (DSM-5) and incontinence in children with attention-deficit/hyperactivity disorder and the controls. Boys n (%) Girls n (%) Mean age in years (SD) Mean IQ (SD) Mean CBCL total T-value (SD) Mean CBCL Ext T-value (SD) Mean CBCL Int T-value (SD) CBCL total score >90th percentile n (%) CBCL Ext score >90th percentile n (%) CBCL Int score >90th percentile n (%) Psychiatric diagnoses Internalizing disordersc n (%) Externalizing disordersd n (%) Incontinence overallb n (%) NE n (%) DUI n (%) FI n (%) Mean LUTS score (SD)
ADHD group (n Z 40)
Control group (n Z 43)
Significancea
30 10 11.4 101.3 65.1 63.6 60.0 23 19 16
(75.0) (25.0) (2.49) (18.66) (8.51) (9.21) (8.49) (57.5) (47.5) (40.0)
26 17 10.7 110.9 47.4 46.1 50.4 1 e 4
n.s.
(10.0) (10.0) (10.0) (5.0) (5.0) (2.5) (1.67)
e
4 4 4 2 2 1 4.3
(60.5) (39.5) (3.03) (15.77) (10.60) (8.46) (9.88) (2.3) (9.3)
1 (2.3) 2 (4.7) e 2 (4.7) e 3.9 (1.52)
n.s. p Z 0.013* p < 0.001* p < 0.001* p < 0.001* p < 0.001* p < 0.001* p Z 0.001*
n.s. n.s. n.s. n.s. n.s.
ADHD Z attention-deficit/hyperactivity disorder; CBCL Z child behavior checklist; CBCL Ext Z CBCL externalizing; CBCL Int Z CBCL internalizing; DUI Z daytime urinary incontinence; FI Z fecal incontinence; NE Z nocturnal enuresis. *Statistical significance at a statistical level of at least p < .05. Bold Z statistically significant result; Italics Z Student t-tests conducted. a Chi-squared test for non-parametric data and t-test for parametric variables. b At least one subtype of incontinence. c Generalized anxiety disorder, specific phobia, separation anxiety disorder. d Conduct disorder, oppositional defiant disorder.
2013), using descriptive statistics, nonparametric (Chisquaredetests, Fisher’s Exact tests) and parametric tests (ttests). Results were considered to be significant at a p-value of 0.05. The local ethics committee approved the study.
Results Descriptive data, incontinence rates, CBCL scores and child psychiatric diagnoses for both groups are shown in Table 1: 10% of the ADHD group were affected by incontinence; two children had NE; one had DUI; and one child had both DUI and FI. Incontinence rates in the control group did not differ significantly: only two children were affected by DUI and none had NE or FI. No significant differences were found regarding the mean LUTS score between the ADHD and control groups (4.3 vs 3.9). No children reached the clinically relevant score of 13. Children with ADHD had a significantly lower IQ (101 vs 111) than the controls (Table 1). Compared to the controls,
Table 2
the ADHD group had significantly more clinically relevant scores in the CBCL total (57.5% vs 2.3%), externalizing and internalizing scale (Table 1). Eight children of the ADHD group (20%) and one control child (2.3%) were diagnosed with a comorbid psychological disorder. Diagnoses in the ADHD group were specific phobia, generalized anxiety disorder, separation anxiety disorder, conduct disorder and oppositional defiant disorder. The control child had oppositional defiant disorder. Incontinence was present in one child with ADHD and a comorbid disorder, but not in the control child with comorbidity. Information on bladder and bowel control is shown in Table 2. Children in the ADHD group reached bladder and bowel control at a mean age of 3.05 years (SD 1.45) during the day, and 3.97 years (SD 2.59) during the night. Children in the control group reached bladder control at a mean age of 2.64 years (SD 0.49) during the day and 3.24 years (SD 0.94) during the night. Bowel control was achieved at a mean age of 2.95 years (SD 1.53) in the ADHD and 2.66 years (SD 0.5) in the control group. The mean ages were slightly
Delayed bladder and bowel control in children with attention-deficit/hyperactivity disorder and the controls.
Delayed daytime bladder control (>5 years) n (%) Delayed nighttime bladder control (>5 years) n (%) Delayed bowel control (>4 years) n (%)
ADHD group (n Z 40)
Control group (n Z 43)
Significance
6 (15.8) 10 (27.0) 9 (27.3)
e 4 (9.3) 3 (7.1)
p Z 0.009*,a p Z 0.037* p Z 0.018*
ADHD, attention-deficit/hyperactivity disorder. *Statistical significance at a statistical level of at least p < .05. a Fisher’s Exact test.
141.e4 higher in the ADHD group, but did not reach statistical significance. However, significantly more children with ADHD had delayed daytime and nighttime bladder control, as well as delayed bowel control, than children in the control group (Table 2). Comparing the inattentive subtype (70%) to the hyperactive/impulsive (10%) and combined subtypes (20%) within the ADHD group, no significant differences were found regarding: incontinence (10.7 vs 8.3%, Fishers Exact test, p Z 1.0); delayed nighttime bladder control (32.0 vs 16.7%, Fishers Exact test, p Z 0.45); daytime bladder control (19.2 vs 8.3%, Fishers Exact test, p Z 0.64); and bowel control (28.6 vs 25.0%; Fishers Exact test, p Z 1.0).
Discussion This is one of the first studies examining incontinence in children who have already received treatment for ADHD. The results indicate that children with an optimal, guideline-oriented treatment of ADHD show no higher rates of incontinence than children without ADHD. In contrast to other findings, incontinence rates in ADHD children in the present study were much lower (NE 5%, DUI 5% and FI 2.5%) than in former studies, especially for NE. One explanation for these low incontinence rates could be that the majority of the ADHD group was already treated with stimulants. This could have had a positive effect on incontinence, as has previously been shown [20]. On the other hand, medication could have improved compliance in the incontinence treatment. In addition, children in the present study received a full child psychiatric assessment, counseling and cognitive-behavioral interventions for ADHD according to evidence-based guidelines. This could also have contributed towards the low rates. However, in this study, incontinence rates at the beginning of ADHD treatment were not assessed. Only longitudinal studies can clarify how far medical treatment with stimulants can affect therapy outcomes of incontinence in children with ADHD. Another explanation for this discrepancy could be the older age of participants. In most of the cited studies, children were younger than in the present study (6e8.7 years vs 11.4 years) [10e12]. Both NE and DUI have spontaneous cure rates e for NE this is up to 15% per year [6]. Older children with ADHD, as examined in the present study, were affected by incontinence in their younger years (up to 27.3% with delayed bladder/bowel control), which had resolved. This explanation is partially supported by Robson et al., who found a significant difference between children with ADHD and controls regarding retrospective NE rates at the age of 6 years, but no difference at the children’s current age (mean 11.2 years) [11]. In that study, NE rates of 3.9% in older children were comparable with those in the present study, whereas DUI rates were still high (13.1%). Only a few studies have assessed the effects of delayed bladder and bowel control in children with ADHD. Although the mean ages of bladder and bowel control did not differ between the groups, the greater standard deviations in the ADHD group indicate a larger variability in reaching continence. Children with ADHD are a more heterogeneous group regarding bladder and bowel control, indicating that
J. Niemczyk et al. subgroups of ADHD patients could be affected by developmental delays and incontinence. In a longitudinal study, children with persisting NE after the age of 10 years had significantly higher risks for attention-deficit, conduct problems and anxiety throughout adolescence than those who achieved continence before the age of 5 years [28]. The greater number of children with delayed bladder and bowel control in the ADHD group could be an indicator for maturational deficits as a common association in incontinence and ADHD. To confirm these findings, age of reaching bladder and bowel control should be assessed in a prospective design. In NE, maturational deficits of the brainstem are assumed, which are supported by findings of arousal deficits and a decreased prepulse inhibition [15]. Additionally, children with NE show a slower motor performance, suggesting maturational deficits in other cortical areas too [29]. Children with ADHD can have deficits in their cognitive processes, attention and motor planning [30] and are also at higher risk of developmental delays (e.g. in motor and speech development and achieving continence) [10]. However, children with ADHD with NE were not more incapacitated than children with ADHD without NE [15]. Research on etiological factors of the association between ADHD and DUI or FI is lacking. Other studies have found that NE is associated more with inattentive than with hyperactive/impulsive ADHD symptoms [16]. In the present study, the majority of the ADHD participants had the inattentive subtype, followed by the combined and hyperactive/impulsive subtype. In population-based samples, most of the ADHD children have the combined subtype (w60%), which is different to the present study [31]. The inattentive subtype is the most difficult to diagnose, as other disorders have to be excluded. The ADHD subtypes were diagnosed by: a full psychiatric assessment, a structured interview, an IQ-test and questionnaires. Despite this detailed assessment, no significant differences between the subtypes could be found, but this could also be explained by the small sample sizes. The present study confirmed that children with ADHD have a high risk for additional behavioral problems. The higher CBCL total, externalizing and internalizing rates in the ADHD group show that these children are not only impaired by attentional, hyperactive and impulsive problems, but also by a variety of additional comorbid psychological problems. These can negatively affect incontinence therapy, outcome and compliance as well. Regarding pharmacological treatment, compliance and outcome rates did not differ between the ADHD children and controls [17]. In NE and/or DUI, drug therapy for incontinence shows satisfactory outcomes in children with ADHD, but lower cure rates than in children without ADHD [18]. In FI, children with ADHD are also at higher risk for a worse treatment outcome [19]. On the other hand, treatment of ADHD, especially medication, can improve treatment outcome of incontinence. As methylphenidate does not seem to have an antienuretic effect, Williamson et al. speculated that stimulants may decrease the sleep arousal threshold and lead to awakening of the child before wetting [20]. The present study shows that in a highly impaired subgroup of children with treated ADHD, incontinence rates
Incontinence in children are relatively low at an older age. Although many of these children reach bladder and bowel control later in life, these problems do not necessarily persist. As evidence-based therapy options are available for both incontinence and ADHD [3,23,24], both should be offered. This underlines the importance of diagnosing both incontinence and comorbid disorders. All children with ADHD should be screened for incontinence when presented in a healthcare setting, just as vice versa, children with incontinence should be screened for comorbid disorders.
Strengths and limitations A major strength of the study was the design including a healthy, matched control group from the community and not a convenience sample. Also, all children were included who presented consecutively at a tertiary care center. All children with ADHD had been diagnosed by both a mentalhealthcare expert and by a structured, standardized diagnostic interview. All children treated for ADHD received a multimodal approach of treatment including behavioral therapy and pharmacotherapy. This study provides first data on the association between treated ADHD, incontinence and bladder/bowel control in psychiatrically treated children compared to controls. A limitation was the heterogeneous group of older ADHD patients differing in subtypes and treatment. Children in the ADHD group also differed in treatment duration for ADHD, and incontinence rates at the beginning of ADHD treatment were not known. Type and duration of ADHD and incontinence treatment were not assessed systematically. The sample was recruited from a tertiary outpatient clinic, which can lead to selection biases. Another limitation was that incontinence was only assessed by parental questionnaires and not by a 48-h voiding diary, uroflowmetry and sonography, which should be considered in future studies. In future studies, the effect and type of ADHD treatment on incontinence rates (before and after ADHD treatment) should be examined in more detail.
Conclusion This study provides further information of the association between ADHD and incontinence. Children with ADHD are not only impaired by problems of attention, hyperactivity and impulsivity, but also by delayed bladder and bowel control. However, in children who are treated for their ADHD according to standard guidelines, incontinence rates are not higher than in children without ADHD. Children with ADHD should be screened for incontinence e and children with incontinence should be screened for ADHD e if symptoms of inattention, hyperactivity or impulsivity are present.
Conflict of interest statement Nil.
Funding Nil.
141.e5
Ethical approval The study was approved by the local ethics committee.
References [1] American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorders, text revision (DSM-IV-TR). Washington, D.C.: American Psychiatric Association; 2000. [2] American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorders e Fifth Edition (DSM 5). Washington, D.C.: APA; 2013. [3] Moriyama TS, Cho AJM, Verin RE, Fuentes J, Polanczyk GV. Attention deficit hyperactivity disorder. In: Rey JM, editor. IACAPAP e-Textbook of Child and Adolescent Mental Health. Geneva: International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http:// iacapap.org/wp-content/uploads/D.1-ADHD-072012.pdf [last accessed 08 October 2014]. [4] Austin PF, Bauer SB, Bower W, Chase J, Franco I, Hoebeke P, et al. The standardization of terminology of lower urinary tract function in children and adolescents: update report from the Standardization Committee of the International Children’s Continence Society. J Urol 2014;191:1863e5. [5] World Health Organization (WHO). The ICD-10 classification of mental and behavioural disorders e diagnostic criteria for research. Geneva: WHO; 1993. [6] Von Gontard A, Neve ´us T. Management of bladder and bowel control in children. London: MacKeith Press; 2006. [7] Joinson C, Heron J, Emond A, Butler R. Psychological problems in children with bedwetting and combined (day and night) wetting: a UK population-based study. J Pediatr Psychol 2007; 32:605e16. [8] Joinson C, Heron J, Von Gontard A. Psychological problems in children with daytime wetting. Pediatrics 2006;118: 1985e93. [9] Joinson C, Heron J, Butler U, Von Gontard A. Psychological differences between children with and without soiling problems. Pediatrics 2006;117:1575e84. [10] Bhatia MS, Nigam VR, Bohra N, Malik SC. Attention deficit disorder with hyperactivity among paediatric outpatients. J Child Psychol Psychiatry Allied Discip 1991;32:297e306. [11] Robson WLM, Jackson HP, Blackhurst D, Leung AKC. Enuresis in children with attention-deficit hyperactivity disorder. South Med J 1997;90:503e5. [12] Yang T, Huang K, Chen S, Chang H, Yang H, Guo Y. Correlation between clinical manifestations of nocturnal enuresis and attentional performance in children with attention deficit hyperactivity disorder (ADHD). J Formos Med Assoc 2013;112: 41e7. [13] Duel BP, Steinberg-Epstein R, Hill M, Lerner M, Koff S, De Gennaro M, et al. A survey of voiding dysfunction in children with attention deficit-hyperactivity disorder. J Urol 2003;170: 1521e4. [14] Mckeown C, Hisle-Gorman E, Eide M, Gorman GH, Nylund CM. Association of constipation and fecal incontinence with attention-deficit/hyperactivity disorder. Pediatrics 2013;132: e1210e5. [15] von Gontard A, Equit M. Comorbidity of ADHD and incontinence in children. Eur Child Adolesc Psychiatry 2015;24: 127e40. [16] Elia J, Takeda T, Deberardinis R, Burke J, Accardo J, Ambrosini PJ, et al. Nocturnal enuresis: a suggestive endophenotype marker for a subgroup of inattentive attention-deficit/hyperactivity disorder. J Pediatr 2009;155: 239e44.
141.e6 [17] Crimmins CR, Rathbun SR, Husmann DA. Management of urinary incontinence and nocturnal enuresis in attention-deficit hyperactivity disorder. J Urol 2003;170:1347e50. [18] Gor RA, Fuhrer J, Schober JM. A retrospective observational study of enuresis, daytime voiding symptoms, and response to medical therapy in children with attention deficit hyperactivity disorder and autism spectrum disorder. J Pediatr Urol 2012;8:314e7. [19] Van Everdingen-Faasen EQ, Gerritsen BJ, Mulder PGH, Fliers EA, Groeneweg M. Psychosocial co-morbidity affects treatment outcome in children with fecal incontinence. Eur J Pediatr 2008;167:985e9. [20] Williamson LB, Gower M, Ulzen T. Enuresis and ADHD in older children and an adolescent treated with stimulant medication: a case series. J Can Acad Child Adolesc Psychiatry 2011; 20:53e5. [21] Schneider S, Margraf J, Unnewehr S. Kinder-DIPS: Diagnostisches Interview bei psychischen Sto ¨rungen von Kindern und Jugendlichen. Berlin: Springer; 1995. [22] Achenbach TM. Manual for the child behavior checklist/4-18 and 1991 profile. Burlington, VT: University of Vermont; 1991. [23] Von Gontard A. Enuresis. In: Rey JM, editor. IACAPAP e-Textbook of Child and Adolescent Mental Health. Geneva: International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http://iacapap.org/wpcontent/uploads/C.4-ENURESIS-072012.pdf [last accessed 08 October 2014]. [24] Von Gontard A. Encopresis. In: Rey JM, editor. IACAPAP eTextbook of Child and Adolescent Mental Health. Geneva:
J. Niemczyk et al.
[25]
[26]
[27] [28]
[29]
[30]
[31]
International Association for Child and Adolescent Psychiatry and Allied Professions; 2012. online: http://iacapap.org/wpcontent/uploads/C.5-ENCOPRESIS-0072012.pdf [last accessed 08 October 2014]. De Gennaro M, Niero M, Capitanucci ML, Von Gontard A, Woodward M, Tubaro A, et al. Validity of the international consultation on incontinence questionnaire-pediatric lower urinary tract symptoms: a screening questionnaire for children. J Urol 2010;184:1662e7. Raven J, Raven JC, Court JH. Raven’s progressive matrices und vocabulary scales. Frankfurt: Harcourt Test Services; 2006. Raven JC. Standard progressive matrices. Go ¨ttingen: BeltzTest; 1998. Fergusson DM, Horwood LJ. Nocturnal enuresis and behavioral problems in adolescence: a 15-year longitudinal study. Pediatrics 1994;94:662e8. von Gontard A, Freitag CM, Seifen S, Pukrop R, Ro ¨hling D. Neuromotor development in nocturnal enuresis. Dev Med Child Neurol 2006;48:744e50. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A 2007;104:19649e54. Elia J, Arcos-Burgos M, Bolton KL, Ambrosini PJ, Berrettini W, Muenke M. ADHD latent class clusters: DSM-IV subtypes and comorbidity. Psychiatry Res 2009;170:192e8.
