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Association of Attention Deficit and Elimination Disorders at School Entry: A Population Based Study
Association of Attention Deficit and Elimination Disorders at School Entry: A Population Based Study A. von Gontard,* A. M. Moritz, S. Thome-Granz and C. Freitag From the Department of Child and Adolescent Psychiatry, Saarland University Hospital (AvG) and Institute for Community Health, Saarpfalz Kreis (AMM, ST-G), Homburg, and Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, J. W. Goethe University, Frankfurt am Main (CF), Germany
Purpose: Attention deficit/hyperactivity disorder is a common comorbid disorder in children with nocturnal enuresis, daytime urinary incontinence and fecal incontinence. We assessed the specific association of these conditions in a population based sample. We hypothesized that children with elimination disorders have a higher rate of attention deficit/hyperactivity disorder, and that children with daytime urinary incontinence are more strongly affected than those with nocturnal enuresis. Materials and Methods: All children in a defined geographic area (Saarpfalz Kreis) were examined at school entry. Mean age was 6.22 years in 734 boys and 6.18 years in 645 girls. A questionnaire regarding elimination problems and the attention problems scale of the Child Behavior Checklist were administered as an interview to parents. Participation rate was 99.1% (1,379 parents). Results: Of the children 71 (5.1%) had attention deficit/hyperactivity disorder problems of clinical relevance (7.1% of boys and 2.9% of girls). A total of 185 children (13.4%) were wet (nocturnal enuresis in 9.1% and daytime urinary incontinence in 4.4%) and 19 (1.4%) had fecal incontinence. Attention deficit/ hyperactivity disorder symptoms were more common in children with urinary incontinence than nonwetting children (16.8% vs 3.4%). When controlled for confounding variables, only children with daytime urinary incontinence (but not nocturnal enuresis) had a significantly higher risk of attention deficit/hyperactivity disorder symptoms (OR 4.4). Conclusions: Attention deficit/hyperactivity disorder symptoms were increased in children with urinary incontinence in this population based sample. Children with daytime urinary incontinence were at greater risk for attention deficit/ hyperactivity disorder than those with nocturnal enuresis. Screening and referral for specialized treatment of both disorders are recommended.
Abbreviations and Acronyms ADHD ⫽ attention deficit/hyperactivity disorder CBCL ⫽ Child Behavior Checklist DI ⫽ daytime urinary incontinence FI ⫽ fecal incontinence NE ⫽ nocturnal enuresis UI ⫽ urinary incontinence Submitted for publication February 15, 2011. Study received local ethics committee approval. * Correspondence: Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany (telephone: 0049-6841-1624395; FAX: 0049-6841-16-24397; e-mail: alexander. [email protected]).
Key Words: attention deficit disorder with hyperactivity; child, preschool; fecal incontinence; nocturnal enuresis; urinary incontinence NOCTURNAL enuresis, diurnal urinary incontinence and fecal incontinence are common disorders of childhood. Of 7-year-old children 10% are wet at night, 2% to 3% are wet during the day and 1% to 3% are affected by soiling.1–3 Elimination disorders are associated with higher rates of emotional and behavioral disorders.3
Epidemiological studies show that 20% to 30% of all children with NE have clinically relevant behavioral problems.3,4 The most specific comorbid disorder in children with NE is ADHD. In a retrospective study of patients with ADHD 20.9% were wet at night (OR 2.7) and 6.5% during the day (OR 4.5).5
0022-5347/11/1865-2027/0 THE JOURNAL OF UROLOGY® © 2011 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION
Vol. 186, 2027-2032, November 2011 Printed in U.S.A. DOI:10.1016/j.juro.2011.07.030
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ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
In an epidemiological study of 8 to 11-year-old children 12.5% of those with NE also had ADHD, compared to 3.6% of children without NE (OR 2.88).6 In another population based study 17.6% of children 7.5 years old with NE had ADHD problems.7 In a clinical setting the comorbidity rate for ADHD and NE was 28% vs approximately 10% in the community.8 At 2 years children with ADHD and enuresis continued to wet much more often (65%) than children with enuresis without ADHD (37%, OR 3.17).9 Enuresis is more difficult to treat in children with ADHD. In a retrospective study 113 children with ADHD and NE had a worse outcome with alarm treatment than those with NE only, with 43% vs 69% dry at 6 months and 19% vs 66% dry at 12 months.10 Noncompliance was reported in 38% of children with ADHD but in only 22% of controls. To ensure an optimal outcome, the comorbid diagnoses of NE and ADHD require special attention and treatment.4 Of children with DI 20% to 40% are affected by comorbid psychological disturbances.3,4 In a large epidemiological cohort of 8,213 children 7.5 to 9 years old those with DI had increased rates of separation anxiety (11.4%), and attention deficit (24.8%), oppositional behavioral (10.9%) and conduct problems (11.8%).11 ADHD also affects treatment outcome in children with DI. In a retrospective analysis 68% of children with DI and ADHD became dry, compared to 91% of children with DI without ADHD.10 Children with FI demonstrate a high rate of internalizing and externalizing disorders (range 30% to 50%).3,4 In an epidemiological study of 8,242 children 7 to 8 years old those with FI had increased rates of separation anxiety (4.3%), specific phobias (4.3%), generalized anxiety (3.4%), ADHD (9.2%) and oppositional defiant disorder (11.9%).12 Children with constipation have the same rate of behavioral problems as children with nonretentive FI.13 Children with FI have more attention problems than controls (20% vs 3%).14 Children with combined FI and UI exhibit even higher rates of comorbid disorders.15 Again, children with FI and behavioral maladjustment are less compliant than those without psychological disorders (71% vs 38%).16 We assessed the specific association of attention deficit disorder and elimination disorders in a population based sample of school-age children. We hypothesized that children with vs without elimination disorders exhibit a higher rate of clinically relevant ADHD problems and that those with DI are more strongly affected than those with NE.
METHODS In the mandatory school entry medical examination for 2006 all 1,391 children in a defined geographic area (Saarpfalz Kreis) were examined by community care
pediatricians. Of the children 1,120 were examined for regular school entry (mean age 6 years) and 207 for potential early entry (5 years), and 64 were reexamined after having been deferred the previous year. Mean ⫾ SD age of the 734 boys was 6.22 ⫾ 0.42 years and that of the 645 girls was 6.18 ⫾ 0.41 years. Ages ranged from 5 years and 1 month to 7 years and 10 months. Mean ages did not differ between the incontinence subgroups. Before school entry examination 3.2% of children had been diagnosed with ADHD. Of these children 20.5% had received medication and 55.5% nonpharmacological treatment (psychotherapy, occupational therapy). Also 7.6% of children had been diagnosed with an elimination disorder. Of these patients 9.5% had received medication and 30.4% nonpharmacological interventions. In addition to the standard pediatric examination and documentation, a questionnaire was administered as a structured interview by the community care pediatricians. A total of 11 parents refused participation and 1 child with a myelomeningocele was excluded. A total of 1,379 questionnaires (99.1%) could be evaluated. The questionnaire included 7 questions regarding elimination problems and 9 questions comprising the attention problems subscale from the CBCL.17 Item 61 of this subscale was omitted (entered as 0), as it did not pertain to preschool children. This omission resulted in a slightly conservative estimation of the true rate of attention problems in this sample. Raw scores and T values based on the German norms were calculated from the remaining 10 items.18 A cutoff at a T value of 67 (raw score greater than 6 in girls and greater than 7 in boys) was used to define clinically relevant ADHD symptoms (borderline plus clinical range). This cutoff is recommended if maximum differentiation is sought between affected and nonaffected children, since it is considered to represent the bottom of the clinical range and corresponds approximately to the 95th percentile.17 Other developmental conditions were diagnosed clinically and documented in a standardized file of the community medicine services. According to this routine clinical appraisal, it was noted if developmental disorders (such as language and coordination disorders) were present, if the family had immigrated to Germany (migration) and if parents were separated (biological parents of child not living together). Recommendations included early, regular and postponed school entry, and special education needs. Other variables, such as socioeconomic status, are not assessed routinely. The study was approved by the local ethics committee. Statistical analyses were performed with SAS®, version 9.2. Descriptive statistics were calculated by chisquare or Fisher’s exact test. Hypotheses were tested by logistic regression models with CBCL attention problems as dependent risk factors and NE, DI and FI as independent risk factors. Age, gender, developmental delay, parental separation and a general indicator for expected problems at school were controlled for as potential confounding variables. In this model the differential effects of the 3 elimination disorders can be described. The independent variables NE and DI (p ⫽ 0.018) as well as DI and FI (p ⬍0.0001) revealed a strong correlation. Therefore, in an additional model these
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Table 1. Frequency of elimination disorders and attention deficit symptoms by gender Disorder Urinary incontinence: NE DI Overall FI (any/encopresis): Isolated With UI Constipation Constipation ⫹ FI ADHD symptoms (clinical/borderline range): Without UI With NE With DI With UI ⫹ FI Overall Totals
No. Girls (%) 41 19 60 9 1 8 4 1
(6.4) (3.0) (9.3) (1.4) (0.2) (1.2) (0.6) (0.2)
8 6 5 4 19
(1.2) (0.9) (0.8) (0.6) (2.9)
1,379 (100)
No. Boys (%)
Total No. (%)
Gender Predominance (p value)*
95 (12.9) 30 (4.1) 125 (17.0) 10 (1.4) 1 (0.1) 9 (1.2) 9 (1.2) 2 (0.3)
136 (9.9) 50 (3.6) 185 (13.4) 19 (1.4) 2 (0.15) 17 (1.2) 13 (0.9) 3 (0.2)
M (⬍0.0001)
32 7 13 5 52
(4.4) (1.0) (1.8) (0.7) (7.1)
645 (100)
40 13 18 9 71
(2.9) (0.9) (1.3) (0.7) (5.1)
M (⬍0.0001)
M
(0.0006)
M
(0.0005)
734 (100)
* All p values were obtained by chi-square or Fisher’s exact test (2-tailed, 1 degree of freedom). Only p values less than 0.05 are shown to indicate gender differences.
risk factors were combined into 1 variable (0 ⫽ no elimination disorder, 1 ⫽ NE present, 2 ⫽ DI with or without NE, 3 ⫽ FI with or without UI). For example, in this variable 14 children with FI and DI were combined with 5 children with FI only. In this second model combined effects of the elimination disorders are described.
RESULTS The frequency of elimination and attentional disorders is outlined in table 1. A total of 185 children were wet at night or during the day. Of the children 19 soiled, while most had a combination of UI and FI. Significantly more boys were affected by any UI or NE but not by DI. Only 1% of the patients had constipation, or approximately a fifth of those with FI. A total of 71 children had clinically relevant ADHD symptoms, of whom 31 had any type of UI and 9 had FI. Again, boys had a significantly higher total rate of ADHD symptoms. Boys and girls did not differ if ADHD was associated with NE, DI or FI. The frequency of elimination disorder symptoms is outlined in table 2. Roughly a third of children had at least 1 episode of NE per week, while approximately half had less than 1 episode per month. These rates were similar for DI but were reversed for FI. Of the children 94% had bowel movements daily, while 1% had bowel movements 1 to 3 times weekly and 1% were constipated. Of the 81 children with frequent (at least once weekly) NE, UI or FI 12%, 58% and 46%, respectively, had ADHD symptoms. In univariate analyses ADHD symptoms were significantly more common in children with UI compared to continent children, and in children with DI compared to those with NE (table 3). Other risk factors were also more common in children with UI.
Signs of a developmental disorder were present in 91 boys and 24 girls, and were more prevalent in children with vs without UI. Although 116 boys and 119 girls came from a different cultural background, there was no significant difference between children with and without UI. Finally, significantly more children (83 boys and 48 girls) with (17%) vs without (8%) UI were from families that had separated. Except for parental separation and migration, children with DI had significantly higher rates of other risk factors than those with NE. Three fourths of all children (549 boys, 508 girls) received a recommendation for mainstream schooling. Table 2. Frequency of incontinence symptoms by gender
NE episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo DI episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo FI episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo Bowel movements: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk
No. Girls (%)
No. Boys (%)
Total No. (%)
6 (14.6) 5 (12.2) 7 (17.1) 10 (24.4) 13 (31.7)
15 (15.8) 7 (7.4) 11 (11.6) 12 (12.6) 50 (52.6)
21 (15.4) 12 (8.8) 18 (13.2) 22 (16.2) 63 (46.3)
4 (21.1) 0 (0) 2 (4.9) 3 (15.9) 10 (52.6)
6 (20.0) 1 (3.3) 6 (20.0) 5 (16.7) 12 (40.0)
10 (20.4) 1 (2.0) 8 (16.3) 8 (16.3) 22 (44.9)
4 (44.4) 2 (22.2) 0 (0) 1 (11.1) 2 (22.2)
4 (40.0) 0 (0) 1 (10.0) 1 (10.0) 4 (40.0)
8 (42.1) 2 (10.5) 1 (5.3) 2 (10.5) 6 (31.6)
594 (92.1) 46 (7.1) 5 (0.8) 0 (0)
700 (95.4) 15 (2.0) 9 (1.2) 0 (0)
1,294 (93.8) 61 (4.4) 14 (1.0) 0 (0)
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ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
Table 3. Univariate analysis of risk factors in children with and without urinary incontinence Urinary Incontinence Status No. Pos (%) ADHD Developmental disorders Migration† Separation‡ School recommendation: Regular entry Early entry Special education§ Delayed/postponed entry㛳 Totals
Urinary Incontinence Type
No. Neg (%)
p Value*
OR (95% CI)
No. DI (%)
No. NE (%)
p Value*
OR (95% CI)
31 (16.8) 44 (23.8) 37 (20.0) 32 (17.3)
40 (3.4) 71 (5.9) 198 (16.6) 99 (8.3)
⬍0.0001 ⬍0.001 0.25 0.0001
5.81 (3.43–9.83) 4.94 (3.19–7.62) 1.26 (0.83–1.89) 2.31 (1.47–3.64)
18 (36.7) 21 (42.9) 4 (8.2) 9 (18.4)
13 (9.6) 23 (16.9) 33 (24.3) 23 (16.9)
⬍0.0001 0.00025 0.015 0.82
5.49 (2.26–13.46) 3.68 (1.68–8.08) 0.28 (0.078–0.89) 1.1 (0.43–2.77)
115 (62.2) 27 (14.6) 10 (5.4) 33 (17.8)
942 (78.9) 144 (12.1) 22 (1.8) 86 (7.2)
⬍0.0001 0.33 0.0027 ⬍0.0001
0.44 (0.31–0.62) 1.25 (0.78–1.98) 3.04 (1.32–6.88) 2.79 (1.77–4.41)
21 (42.9) 5 (10.2) 6 (12.2) 17 (34.7)
94 (69.1) 22 (16.2) 4 (2.9) 16 (11.8)
0.001 0.31 0.013 0.0003
0.33 (0.16–0.69) 0.59 (0.18–1.78) 4.60 (1.08–20.58) 3.98 (1.69–9.42)
185 (100)
1,194 (100)
49 (100)
136 (100)
* Chi-square test (1 degree of freedom). † Any immigration to Germany. ‡ Biological parents of child not living together. § Includes children who will enter mainstream school with aid of special teacher or will enter special school directly (Förderschule). 㛳 Includes younger children who did not receive recommendation for early school entry.
This rate was lower in children with vs without UI. Early school entry was recommended for roughly a tenth of the children (79 boys, 92 girls), with no differences between those with and without UI. Special education was recommended for 2% of children (20 boys, 12 girls), and this rate was higher in children with vs without UI. For almost a tenth of children (86 boys, 33 girls) delayed or postponed school entry was advised, and again this rate was higher in children with vs without UI. Children with DI had significantly more special education needs or delayed school entry compared to those with NE (table 3). In multivariate analyses ADHD symptoms were more common in children with DI when NE and FI were controlled for (table 4). The model correctly predicted 91% of all cases with clinically relevant ADHD symptoms. Notably NE or FI alone did not pose a strong risk for ADHD symptoms, but DI showed a fourfold increased risk (OR 4.4). When all elimination disorders were combined in 1 categorical Table 4. Risk factors for clinically relevant CBCL inattentive scale symptom scores Independent Variable
Wald Chi-Square
p Value
OR (95% CI)
NE DI FI Age Gender Developmental disorder Migration Separation Expected problems in school*
3.1 8.3 0.2 1.3 0.0 42.7 0.0 11.9 9.9
0.080 0.004 0.688 0.249 0.970 ⬍0.0001 0.858 0.0006 0.002
2.0 (0.9–4.4) 4.4 (1.6–12.0) 1.3 (0.3–5.5) 1.4 (0.8–2.6) 1.0 (0.5–2.0) 9.6 (4.9–18.9) 0.9 (0.4–2.1) 3.3 (1.7–6.7) 4.1 (1.7–10.0)
Multivariate analyses (logistic regression) were controlled for age, gender, developmental disorder, parental migration, parental separation and expected problems in school. * Includes special education/delayed and postponed school entry.
variable in the same model, this variable again demonstrated a strong association with ADHD symptoms (p ⫽ 0.002). Nighttime wetting (without DI or FI) was not associated with ADHD symptoms (OR 1.9, 95% CI 0.9 – 4.3), but DI (with or without nighttime wetting) and FI (with or without nighttime or daytime wetting) were strongly associated (DI OR 4.6, 95% CI 1.6 –13.0; FI OR 4.9, 95% CI 1.5–15.9).
DISCUSSION This study is among the few epidemiological series focusing on the specific associations of UI and ADHD symptoms. Since the questionnaires were administered as a structured interview by the examining pediatricians, the reliability of answers can be considered high and the data complete. With a participation rate of 99.1% the results are highly representative. The rates of NE, DI and FI for age 6 years were comparable to other epidemiological studies.3 International Children’s Continence Society terminology was used.1 However, the society does not define the frequency of incontinence episodes required for a diagnosis. Depending on the severity, different prevalence rates will evolve. For NE 62 of 1,379 patients (4.5%) fulfilled the ICD-10 research criteria requiring at least 1 episode monthly.19 The prevalence rate of 13.4% decreased further to 3.6% (50 patients) with a definition of at least 1 episode weekly and to 2.3% (32) with stricter definitions (50% wet nights in 2 weeks).20 ADHD symptoms were more common in children with frequent incontinence, which is in keeping with other population based studies.7,11,12 The prevalence of constipation was much lower than in other studies, suggestive of parental under-
ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
reporting.21 Parents seem to be less aware of the signs of constipation than the more obvious and distressing symptoms of FI. With 5.1% of children affected the prevalence of ADHD symptoms is comparable to other studies.22 Diagnoses such as ADHD cannot be derived from questionnaires alone. The CBCL is one of the best validated and most widely used questionnaires, enabling a direct comparison with normal values in many countries.17,18 This tool displays a high construct validity and, therefore, its use in epidemiological research is justified. Boys were more affected than girls regarding NE and ADHD symptoms, which is in accordance with other studies.3 However, no gender differences were reported for DI and FI, in contrast to other studies showing a clear predominance of boys with FI.12,13 Using multivariate analyses, the specific risks of ADHD problems in each elimination disorder were calculated. Only DI was specifically associated with ADHD symptoms in this sample. Possibly subgroups of NE, such as nonmonosymptomatic or secondary NE, exhibit a stronger association with ADHD symptoms. Neither NE nor FI posed an additional risk of ADHD symptoms when DI and several important confounding factors were controlled for. Among these factors the most prominent was developmental delay. FI increased the risk of ADHD symptoms only in combination with DI but was not respectively controlled for when DI was not present. This study reveals that NE is not a specific risk factor for ADHD symptoms when psychosocial risk factors (parental separation) and developmental delay are controlled for. Previous studies describing higher comorbidity rates of NE and ADHD may have
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included more children with developmental delay without controlling for this confounding factor.6 – 8 Children with DI are at much higher risk for ADHD, as reported previously.11 These findings are in congruence with the multifactorial etiologies of ADHD and UI, by which similar factors interact with each other in both disorders. In UI genetic factors are modulated by stressful life events (such as separation of parents), developmental disorders (such as motor problems and postponed school entry) and comorbid disturbances.23–25 Genetic factors and developmental and comorbid disorders are also involved in ADHD.22
CONCLUSIONS In clinical practice children with UI and ADHD have a much lower response rate to treatment than those with incontinence alone due to a lower compliance.9,10 It is important that ADHD be diagnosed and treated in accordance with current standards, in addition to incontinence treatment.22 Many children had an existing diagnosis of ADHD in this study and had even received treatment, although ADHD treatment in preschool children requires special care due to increased rates of side effects of stimulants.26 Since children can be affected by many other comorbid disorders in addition to ADHD, screening of all children with incontinence with broadband, standardized questionnaires such as the CBCL is recommended.4 This questionnaire can be completed by parents within 20 minutes.17,18 Even shorter screening instruments with 11 questions have been developed.27 If ADHD and other disorders are suspected, referral to specialized mental health services for children is recommended.4
REFERENCES 1. Nevéus T, von Gontard A, Hoebeke P et al: The standardization of terminology of lower urinary tract function in children and adolescents: report from the Standardisation Committee of the International Children’s Continence Society. J Urol 2006; 176: 314.
6. Shreeram A, Jian-Ping HE, Kalaydijan A et al: Prevalence of enuresis and its association with attention-deficit/hyperactivity disorder among U.S. children: results from a nationally representative study. J Am Acad Child Adolesc Psychiatry 2009; 48: 35.
2. Rasquin A, Di Lorenzo C, Forbes D et al: Childhood functional gastrointestinal disorders: child/ adolescent. Gastroenterology 2006; 130: 1527.
7. Joinson C, Heron J, Emond A et al: Psychological problems in children with bedwetting and combined (day and night) wetting: a UK populationbased study. J Pediatr Psychol 2007; 32: 605.
3. von Gontard A and Nevéus T: Management of Disorders of Bladder and Bowel Control in Childhood. London: MacKeith Press 2006. 4. von Gontard A, Baeyens D, Van Hoecke E et al: Psychological and psychiatric issues in urinary and fecal incontinence. J Urol 2011; 185: 1432. 5. Robson WL, Jackson HP, Blackhurst D et al: Enuresis in children with attention-deficit hyperactivity disorder. South Med J 1997; 90: 503.
8. Baeyens D, Roeyers H, D’Haese L et al: The prevalence of ADHD in children with enuresis: comparison between samples of primary care and pediatric clinic. Acta Paediatr 2006; 95: 347. 9. Baeyens D, Roeyers H, Demeyere I et al: Attention-deficit/hyperactivity disorder (ADHD) as a risk factor for difficult to cure nocturnal enuresis in children: a two-year follow-up study. Acta Paediatr 2005; 94: 1619.
10. Crimmins CR, Rathburn SR and Husman DA: Management of urinary incontinence and nocturnal enuresis in attention-deficit hyperactivity disorder. J Urol 2003; 170: 1347. 11. Joinson C, Heron J, von Gontard A et al: Psychological problems in children with daytime wetting. Pediatrics 2006; 118: 1985. 12. Joinson C, Heron J, Butler U et al: Psychological differences between children with and without soiling problems. Pediatrics 2006; 117: 1575. 13. Benninga MA, Buller HA, Heymans HS et al: Is encopresis always the result of constipation? Arch Dis Child 1994; 71: 186. 14. Cox DJ, Morris JB, Borrowitz SM et al: Psychological differences between children with and without chronic encopresis. J Pediatr Psychol 2002; 27: 585.
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15. von Gontard A and Hollmann E: Comorbidity of functional urinary incontinence and encopresis: somatic and behavioral associations. J Urol 2004; 171: 2644. 16. Nolan T, Debelle G, Oberklaid F et al: Randomised trial of laxatives in treatment of childhood encopresis. Lancet 1991; 338: 523. 17. Achenbach TM: Manual for the Child Behavior Checklist 4-18, 1991 Profile. Burlington: University of Vermont 1991. 18. Arbeitsgruppe Deutsche Child Behavior Checklist. Deutsche Bearbeitung der Child Behavior Checklist (CBCL/4-18): Einführung und Anleitung zur Handauswertung, 2. Auflage mit deutschen Normen. Koeln: Arbeitsgruppe Kinder-, Jugend- und Familiendiagnostik 1999. 19. World Health Organization: The ICD-10 Classification of Mental and Behavioural Disorders. Di-
agnostic Criteria for Research. Geneva: World Health Organization 1993. 20. Butler RJ: Etablishment of working definitions in nocturnal enuresis. Arch Dis Child 1991; 66: 267. 21. van den Berg MM, Benninga MA and Di Lorenzo C: Epidemiology of childhood constipation: a systematic review. Am J Gastroenterol 2006; 101: 2401. 22. Pliszka S; AACAP Work Group on Quality Issues: Practice parameter for the assessment and treatment of children and adolescents with attentiondeficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2007; 46: 894. 23. Elia J, Takeda T, Deberardinis R et al: Nocturnal enuresis: a suggestive endophenotype marker for a subgroup on inattentive attention-deficit/hyperactivity disorder. J Pediatr 2009; 155: 239.
24. Järvelin MR, Moilanen I, Vikeväinen-Tervonen L et al: Life changes and protective capacities in enuretic and non-enuretic children. J Child Psychol Psychiatry 1990; 31: 763. 25. Järvelin MR, Vikeväinen-Tervonen L, Moilanen I et al: Enuresis in seven-year-old children. Acta Paediatr Scand 1988; 77: 148. 26. Wigal T, Greenhill L, Chuang S et al: Safety and tolerability of methylphenidate in preschool children with ADHD. J Am Acad Child Adolesc Psychiatry 2006; 45: 1294. 27. Van Hoecke E, Baeyens D, Vanden Bossche H et al: Early detection of psychological problems in a population of children with enuresis: construction and validation of the short screening instrument for psychological problems in enuresis. J Urol 2007; 178: 2611.
Purpose: Attention deficit/hyperactivity disorder is a common comorbid disorder in children with nocturnal enuresis, daytime urinary incontinence and fecal incontinence. We assessed the specific association of these conditions in a population based sample. We hypothesized that children with elimination disorders have a higher rate of attention deficit/hyperactivity disorder, and that children with daytime urinary incontinence are more strongly affected than those with nocturnal enuresis. Materials and Methods: All children in a defined geographic area (Saarpfalz Kreis) were examined at school entry. Mean age was 6.22 years in 734 boys and 6.18 years in 645 girls. A questionnaire regarding elimination problems and the attention problems scale of the Child Behavior Checklist were administered as an interview to parents. Participation rate was 99.1% (1,379 parents). Results: Of the children 71 (5.1%) had attention deficit/hyperactivity disorder problems of clinical relevance (7.1% of boys and 2.9% of girls). A total of 185 children (13.4%) were wet (nocturnal enuresis in 9.1% and daytime urinary incontinence in 4.4%) and 19 (1.4%) had fecal incontinence. Attention deficit/ hyperactivity disorder symptoms were more common in children with urinary incontinence than nonwetting children (16.8% vs 3.4%). When controlled for confounding variables, only children with daytime urinary incontinence (but not nocturnal enuresis) had a significantly higher risk of attention deficit/hyperactivity disorder symptoms (OR 4.4). Conclusions: Attention deficit/hyperactivity disorder symptoms were increased in children with urinary incontinence in this population based sample. Children with daytime urinary incontinence were at greater risk for attention deficit/ hyperactivity disorder than those with nocturnal enuresis. Screening and referral for specialized treatment of both disorders are recommended.
Abbreviations and Acronyms ADHD ⫽ attention deficit/hyperactivity disorder CBCL ⫽ Child Behavior Checklist DI ⫽ daytime urinary incontinence FI ⫽ fecal incontinence NE ⫽ nocturnal enuresis UI ⫽ urinary incontinence Submitted for publication February 15, 2011. Study received local ethics committee approval. * Correspondence: Department of Child and Adolescent Psychiatry, Saarland University Hospital, 66421 Homburg, Germany (telephone: 0049-6841-1624395; FAX: 0049-6841-16-24397; e-mail: alexander. [email protected]).
Key Words: attention deficit disorder with hyperactivity; child, preschool; fecal incontinence; nocturnal enuresis; urinary incontinence NOCTURNAL enuresis, diurnal urinary incontinence and fecal incontinence are common disorders of childhood. Of 7-year-old children 10% are wet at night, 2% to 3% are wet during the day and 1% to 3% are affected by soiling.1–3 Elimination disorders are associated with higher rates of emotional and behavioral disorders.3
Epidemiological studies show that 20% to 30% of all children with NE have clinically relevant behavioral problems.3,4 The most specific comorbid disorder in children with NE is ADHD. In a retrospective study of patients with ADHD 20.9% were wet at night (OR 2.7) and 6.5% during the day (OR 4.5).5
0022-5347/11/1865-2027/0 THE JOURNAL OF UROLOGY® © 2011 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION
Vol. 186, 2027-2032, November 2011 Printed in U.S.A. DOI:10.1016/j.juro.2011.07.030
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RESEARCH, INC.
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ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
In an epidemiological study of 8 to 11-year-old children 12.5% of those with NE also had ADHD, compared to 3.6% of children without NE (OR 2.88).6 In another population based study 17.6% of children 7.5 years old with NE had ADHD problems.7 In a clinical setting the comorbidity rate for ADHD and NE was 28% vs approximately 10% in the community.8 At 2 years children with ADHD and enuresis continued to wet much more often (65%) than children with enuresis without ADHD (37%, OR 3.17).9 Enuresis is more difficult to treat in children with ADHD. In a retrospective study 113 children with ADHD and NE had a worse outcome with alarm treatment than those with NE only, with 43% vs 69% dry at 6 months and 19% vs 66% dry at 12 months.10 Noncompliance was reported in 38% of children with ADHD but in only 22% of controls. To ensure an optimal outcome, the comorbid diagnoses of NE and ADHD require special attention and treatment.4 Of children with DI 20% to 40% are affected by comorbid psychological disturbances.3,4 In a large epidemiological cohort of 8,213 children 7.5 to 9 years old those with DI had increased rates of separation anxiety (11.4%), and attention deficit (24.8%), oppositional behavioral (10.9%) and conduct problems (11.8%).11 ADHD also affects treatment outcome in children with DI. In a retrospective analysis 68% of children with DI and ADHD became dry, compared to 91% of children with DI without ADHD.10 Children with FI demonstrate a high rate of internalizing and externalizing disorders (range 30% to 50%).3,4 In an epidemiological study of 8,242 children 7 to 8 years old those with FI had increased rates of separation anxiety (4.3%), specific phobias (4.3%), generalized anxiety (3.4%), ADHD (9.2%) and oppositional defiant disorder (11.9%).12 Children with constipation have the same rate of behavioral problems as children with nonretentive FI.13 Children with FI have more attention problems than controls (20% vs 3%).14 Children with combined FI and UI exhibit even higher rates of comorbid disorders.15 Again, children with FI and behavioral maladjustment are less compliant than those without psychological disorders (71% vs 38%).16 We assessed the specific association of attention deficit disorder and elimination disorders in a population based sample of school-age children. We hypothesized that children with vs without elimination disorders exhibit a higher rate of clinically relevant ADHD problems and that those with DI are more strongly affected than those with NE.
METHODS In the mandatory school entry medical examination for 2006 all 1,391 children in a defined geographic area (Saarpfalz Kreis) were examined by community care
pediatricians. Of the children 1,120 were examined for regular school entry (mean age 6 years) and 207 for potential early entry (5 years), and 64 were reexamined after having been deferred the previous year. Mean ⫾ SD age of the 734 boys was 6.22 ⫾ 0.42 years and that of the 645 girls was 6.18 ⫾ 0.41 years. Ages ranged from 5 years and 1 month to 7 years and 10 months. Mean ages did not differ between the incontinence subgroups. Before school entry examination 3.2% of children had been diagnosed with ADHD. Of these children 20.5% had received medication and 55.5% nonpharmacological treatment (psychotherapy, occupational therapy). Also 7.6% of children had been diagnosed with an elimination disorder. Of these patients 9.5% had received medication and 30.4% nonpharmacological interventions. In addition to the standard pediatric examination and documentation, a questionnaire was administered as a structured interview by the community care pediatricians. A total of 11 parents refused participation and 1 child with a myelomeningocele was excluded. A total of 1,379 questionnaires (99.1%) could be evaluated. The questionnaire included 7 questions regarding elimination problems and 9 questions comprising the attention problems subscale from the CBCL.17 Item 61 of this subscale was omitted (entered as 0), as it did not pertain to preschool children. This omission resulted in a slightly conservative estimation of the true rate of attention problems in this sample. Raw scores and T values based on the German norms were calculated from the remaining 10 items.18 A cutoff at a T value of 67 (raw score greater than 6 in girls and greater than 7 in boys) was used to define clinically relevant ADHD symptoms (borderline plus clinical range). This cutoff is recommended if maximum differentiation is sought between affected and nonaffected children, since it is considered to represent the bottom of the clinical range and corresponds approximately to the 95th percentile.17 Other developmental conditions were diagnosed clinically and documented in a standardized file of the community medicine services. According to this routine clinical appraisal, it was noted if developmental disorders (such as language and coordination disorders) were present, if the family had immigrated to Germany (migration) and if parents were separated (biological parents of child not living together). Recommendations included early, regular and postponed school entry, and special education needs. Other variables, such as socioeconomic status, are not assessed routinely. The study was approved by the local ethics committee. Statistical analyses were performed with SAS®, version 9.2. Descriptive statistics were calculated by chisquare or Fisher’s exact test. Hypotheses were tested by logistic regression models with CBCL attention problems as dependent risk factors and NE, DI and FI as independent risk factors. Age, gender, developmental delay, parental separation and a general indicator for expected problems at school were controlled for as potential confounding variables. In this model the differential effects of the 3 elimination disorders can be described. The independent variables NE and DI (p ⫽ 0.018) as well as DI and FI (p ⬍0.0001) revealed a strong correlation. Therefore, in an additional model these
ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
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Table 1. Frequency of elimination disorders and attention deficit symptoms by gender Disorder Urinary incontinence: NE DI Overall FI (any/encopresis): Isolated With UI Constipation Constipation ⫹ FI ADHD symptoms (clinical/borderline range): Without UI With NE With DI With UI ⫹ FI Overall Totals
No. Girls (%) 41 19 60 9 1 8 4 1
(6.4) (3.0) (9.3) (1.4) (0.2) (1.2) (0.6) (0.2)
8 6 5 4 19
(1.2) (0.9) (0.8) (0.6) (2.9)
1,379 (100)
No. Boys (%)
Total No. (%)
Gender Predominance (p value)*
95 (12.9) 30 (4.1) 125 (17.0) 10 (1.4) 1 (0.1) 9 (1.2) 9 (1.2) 2 (0.3)
136 (9.9) 50 (3.6) 185 (13.4) 19 (1.4) 2 (0.15) 17 (1.2) 13 (0.9) 3 (0.2)
M (⬍0.0001)
32 7 13 5 52
(4.4) (1.0) (1.8) (0.7) (7.1)
645 (100)
40 13 18 9 71
(2.9) (0.9) (1.3) (0.7) (5.1)
M (⬍0.0001)
M
(0.0006)
M
(0.0005)
734 (100)
* All p values were obtained by chi-square or Fisher’s exact test (2-tailed, 1 degree of freedom). Only p values less than 0.05 are shown to indicate gender differences.
risk factors were combined into 1 variable (0 ⫽ no elimination disorder, 1 ⫽ NE present, 2 ⫽ DI with or without NE, 3 ⫽ FI with or without UI). For example, in this variable 14 children with FI and DI were combined with 5 children with FI only. In this second model combined effects of the elimination disorders are described.
RESULTS The frequency of elimination and attentional disorders is outlined in table 1. A total of 185 children were wet at night or during the day. Of the children 19 soiled, while most had a combination of UI and FI. Significantly more boys were affected by any UI or NE but not by DI. Only 1% of the patients had constipation, or approximately a fifth of those with FI. A total of 71 children had clinically relevant ADHD symptoms, of whom 31 had any type of UI and 9 had FI. Again, boys had a significantly higher total rate of ADHD symptoms. Boys and girls did not differ if ADHD was associated with NE, DI or FI. The frequency of elimination disorder symptoms is outlined in table 2. Roughly a third of children had at least 1 episode of NE per week, while approximately half had less than 1 episode per month. These rates were similar for DI but were reversed for FI. Of the children 94% had bowel movements daily, while 1% had bowel movements 1 to 3 times weekly and 1% were constipated. Of the 81 children with frequent (at least once weekly) NE, UI or FI 12%, 58% and 46%, respectively, had ADHD symptoms. In univariate analyses ADHD symptoms were significantly more common in children with UI compared to continent children, and in children with DI compared to those with NE (table 3). Other risk factors were also more common in children with UI.
Signs of a developmental disorder were present in 91 boys and 24 girls, and were more prevalent in children with vs without UI. Although 116 boys and 119 girls came from a different cultural background, there was no significant difference between children with and without UI. Finally, significantly more children (83 boys and 48 girls) with (17%) vs without (8%) UI were from families that had separated. Except for parental separation and migration, children with DI had significantly higher rates of other risk factors than those with NE. Three fourths of all children (549 boys, 508 girls) received a recommendation for mainstream schooling. Table 2. Frequency of incontinence symptoms by gender
NE episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo DI episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo FI episodes: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk Fewer than 1/mo Bowel movements: 7/Wk 4–6/Wk 1–3/Wk Fewer than 1/wk
No. Girls (%)
No. Boys (%)
Total No. (%)
6 (14.6) 5 (12.2) 7 (17.1) 10 (24.4) 13 (31.7)
15 (15.8) 7 (7.4) 11 (11.6) 12 (12.6) 50 (52.6)
21 (15.4) 12 (8.8) 18 (13.2) 22 (16.2) 63 (46.3)
4 (21.1) 0 (0) 2 (4.9) 3 (15.9) 10 (52.6)
6 (20.0) 1 (3.3) 6 (20.0) 5 (16.7) 12 (40.0)
10 (20.4) 1 (2.0) 8 (16.3) 8 (16.3) 22 (44.9)
4 (44.4) 2 (22.2) 0 (0) 1 (11.1) 2 (22.2)
4 (40.0) 0 (0) 1 (10.0) 1 (10.0) 4 (40.0)
8 (42.1) 2 (10.5) 1 (5.3) 2 (10.5) 6 (31.6)
594 (92.1) 46 (7.1) 5 (0.8) 0 (0)
700 (95.4) 15 (2.0) 9 (1.2) 0 (0)
1,294 (93.8) 61 (4.4) 14 (1.0) 0 (0)
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ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
Table 3. Univariate analysis of risk factors in children with and without urinary incontinence Urinary Incontinence Status No. Pos (%) ADHD Developmental disorders Migration† Separation‡ School recommendation: Regular entry Early entry Special education§ Delayed/postponed entry㛳 Totals
Urinary Incontinence Type
No. Neg (%)
p Value*
OR (95% CI)
No. DI (%)
No. NE (%)
p Value*
OR (95% CI)
31 (16.8) 44 (23.8) 37 (20.0) 32 (17.3)
40 (3.4) 71 (5.9) 198 (16.6) 99 (8.3)
⬍0.0001 ⬍0.001 0.25 0.0001
5.81 (3.43–9.83) 4.94 (3.19–7.62) 1.26 (0.83–1.89) 2.31 (1.47–3.64)
18 (36.7) 21 (42.9) 4 (8.2) 9 (18.4)
13 (9.6) 23 (16.9) 33 (24.3) 23 (16.9)
⬍0.0001 0.00025 0.015 0.82
5.49 (2.26–13.46) 3.68 (1.68–8.08) 0.28 (0.078–0.89) 1.1 (0.43–2.77)
115 (62.2) 27 (14.6) 10 (5.4) 33 (17.8)
942 (78.9) 144 (12.1) 22 (1.8) 86 (7.2)
⬍0.0001 0.33 0.0027 ⬍0.0001
0.44 (0.31–0.62) 1.25 (0.78–1.98) 3.04 (1.32–6.88) 2.79 (1.77–4.41)
21 (42.9) 5 (10.2) 6 (12.2) 17 (34.7)
94 (69.1) 22 (16.2) 4 (2.9) 16 (11.8)
0.001 0.31 0.013 0.0003
0.33 (0.16–0.69) 0.59 (0.18–1.78) 4.60 (1.08–20.58) 3.98 (1.69–9.42)
185 (100)
1,194 (100)
49 (100)
136 (100)
* Chi-square test (1 degree of freedom). † Any immigration to Germany. ‡ Biological parents of child not living together. § Includes children who will enter mainstream school with aid of special teacher or will enter special school directly (Förderschule). 㛳 Includes younger children who did not receive recommendation for early school entry.
This rate was lower in children with vs without UI. Early school entry was recommended for roughly a tenth of the children (79 boys, 92 girls), with no differences between those with and without UI. Special education was recommended for 2% of children (20 boys, 12 girls), and this rate was higher in children with vs without UI. For almost a tenth of children (86 boys, 33 girls) delayed or postponed school entry was advised, and again this rate was higher in children with vs without UI. Children with DI had significantly more special education needs or delayed school entry compared to those with NE (table 3). In multivariate analyses ADHD symptoms were more common in children with DI when NE and FI were controlled for (table 4). The model correctly predicted 91% of all cases with clinically relevant ADHD symptoms. Notably NE or FI alone did not pose a strong risk for ADHD symptoms, but DI showed a fourfold increased risk (OR 4.4). When all elimination disorders were combined in 1 categorical Table 4. Risk factors for clinically relevant CBCL inattentive scale symptom scores Independent Variable
Wald Chi-Square
p Value
OR (95% CI)
NE DI FI Age Gender Developmental disorder Migration Separation Expected problems in school*
3.1 8.3 0.2 1.3 0.0 42.7 0.0 11.9 9.9
0.080 0.004 0.688 0.249 0.970 ⬍0.0001 0.858 0.0006 0.002
2.0 (0.9–4.4) 4.4 (1.6–12.0) 1.3 (0.3–5.5) 1.4 (0.8–2.6) 1.0 (0.5–2.0) 9.6 (4.9–18.9) 0.9 (0.4–2.1) 3.3 (1.7–6.7) 4.1 (1.7–10.0)
Multivariate analyses (logistic regression) were controlled for age, gender, developmental disorder, parental migration, parental separation and expected problems in school. * Includes special education/delayed and postponed school entry.
variable in the same model, this variable again demonstrated a strong association with ADHD symptoms (p ⫽ 0.002). Nighttime wetting (without DI or FI) was not associated with ADHD symptoms (OR 1.9, 95% CI 0.9 – 4.3), but DI (with or without nighttime wetting) and FI (with or without nighttime or daytime wetting) were strongly associated (DI OR 4.6, 95% CI 1.6 –13.0; FI OR 4.9, 95% CI 1.5–15.9).
DISCUSSION This study is among the few epidemiological series focusing on the specific associations of UI and ADHD symptoms. Since the questionnaires were administered as a structured interview by the examining pediatricians, the reliability of answers can be considered high and the data complete. With a participation rate of 99.1% the results are highly representative. The rates of NE, DI and FI for age 6 years were comparable to other epidemiological studies.3 International Children’s Continence Society terminology was used.1 However, the society does not define the frequency of incontinence episodes required for a diagnosis. Depending on the severity, different prevalence rates will evolve. For NE 62 of 1,379 patients (4.5%) fulfilled the ICD-10 research criteria requiring at least 1 episode monthly.19 The prevalence rate of 13.4% decreased further to 3.6% (50 patients) with a definition of at least 1 episode weekly and to 2.3% (32) with stricter definitions (50% wet nights in 2 weeks).20 ADHD symptoms were more common in children with frequent incontinence, which is in keeping with other population based studies.7,11,12 The prevalence of constipation was much lower than in other studies, suggestive of parental under-
ATTENTION DEFICIT AND ELIMINATION DISORDERS AT SCHOOL ENTRY
reporting.21 Parents seem to be less aware of the signs of constipation than the more obvious and distressing symptoms of FI. With 5.1% of children affected the prevalence of ADHD symptoms is comparable to other studies.22 Diagnoses such as ADHD cannot be derived from questionnaires alone. The CBCL is one of the best validated and most widely used questionnaires, enabling a direct comparison with normal values in many countries.17,18 This tool displays a high construct validity and, therefore, its use in epidemiological research is justified. Boys were more affected than girls regarding NE and ADHD symptoms, which is in accordance with other studies.3 However, no gender differences were reported for DI and FI, in contrast to other studies showing a clear predominance of boys with FI.12,13 Using multivariate analyses, the specific risks of ADHD problems in each elimination disorder were calculated. Only DI was specifically associated with ADHD symptoms in this sample. Possibly subgroups of NE, such as nonmonosymptomatic or secondary NE, exhibit a stronger association with ADHD symptoms. Neither NE nor FI posed an additional risk of ADHD symptoms when DI and several important confounding factors were controlled for. Among these factors the most prominent was developmental delay. FI increased the risk of ADHD symptoms only in combination with DI but was not respectively controlled for when DI was not present. This study reveals that NE is not a specific risk factor for ADHD symptoms when psychosocial risk factors (parental separation) and developmental delay are controlled for. Previous studies describing higher comorbidity rates of NE and ADHD may have
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included more children with developmental delay without controlling for this confounding factor.6 – 8 Children with DI are at much higher risk for ADHD, as reported previously.11 These findings are in congruence with the multifactorial etiologies of ADHD and UI, by which similar factors interact with each other in both disorders. In UI genetic factors are modulated by stressful life events (such as separation of parents), developmental disorders (such as motor problems and postponed school entry) and comorbid disturbances.23–25 Genetic factors and developmental and comorbid disorders are also involved in ADHD.22
CONCLUSIONS In clinical practice children with UI and ADHD have a much lower response rate to treatment than those with incontinence alone due to a lower compliance.9,10 It is important that ADHD be diagnosed and treated in accordance with current standards, in addition to incontinence treatment.22 Many children had an existing diagnosis of ADHD in this study and had even received treatment, although ADHD treatment in preschool children requires special care due to increased rates of side effects of stimulants.26 Since children can be affected by many other comorbid disorders in addition to ADHD, screening of all children with incontinence with broadband, standardized questionnaires such as the CBCL is recommended.4 This questionnaire can be completed by parents within 20 minutes.17,18 Even shorter screening instruments with 11 questions have been developed.27 If ADHD and other disorders are suspected, referral to specialized mental health services for children is recommended.4
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6. Shreeram A, Jian-Ping HE, Kalaydijan A et al: Prevalence of enuresis and its association with attention-deficit/hyperactivity disorder among U.S. children: results from a nationally representative study. J Am Acad Child Adolesc Psychiatry 2009; 48: 35.
2. Rasquin A, Di Lorenzo C, Forbes D et al: Childhood functional gastrointestinal disorders: child/ adolescent. Gastroenterology 2006; 130: 1527.
7. Joinson C, Heron J, Emond A et al: Psychological problems in children with bedwetting and combined (day and night) wetting: a UK populationbased study. J Pediatr Psychol 2007; 32: 605.
3. von Gontard A and Nevéus T: Management of Disorders of Bladder and Bowel Control in Childhood. London: MacKeith Press 2006. 4. von Gontard A, Baeyens D, Van Hoecke E et al: Psychological and psychiatric issues in urinary and fecal incontinence. J Urol 2011; 185: 1432. 5. Robson WL, Jackson HP, Blackhurst D et al: Enuresis in children with attention-deficit hyperactivity disorder. South Med J 1997; 90: 503.
8. Baeyens D, Roeyers H, D’Haese L et al: The prevalence of ADHD in children with enuresis: comparison between samples of primary care and pediatric clinic. Acta Paediatr 2006; 95: 347. 9. Baeyens D, Roeyers H, Demeyere I et al: Attention-deficit/hyperactivity disorder (ADHD) as a risk factor for difficult to cure nocturnal enuresis in children: a two-year follow-up study. Acta Paediatr 2005; 94: 1619.
10. Crimmins CR, Rathburn SR and Husman DA: Management of urinary incontinence and nocturnal enuresis in attention-deficit hyperactivity disorder. J Urol 2003; 170: 1347. 11. Joinson C, Heron J, von Gontard A et al: Psychological problems in children with daytime wetting. Pediatrics 2006; 118: 1985. 12. Joinson C, Heron J, Butler U et al: Psychological differences between children with and without soiling problems. Pediatrics 2006; 117: 1575. 13. Benninga MA, Buller HA, Heymans HS et al: Is encopresis always the result of constipation? Arch Dis Child 1994; 71: 186. 14. Cox DJ, Morris JB, Borrowitz SM et al: Psychological differences between children with and without chronic encopresis. J Pediatr Psychol 2002; 27: 585.
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15. von Gontard A and Hollmann E: Comorbidity of functional urinary incontinence and encopresis: somatic and behavioral associations. J Urol 2004; 171: 2644. 16. Nolan T, Debelle G, Oberklaid F et al: Randomised trial of laxatives in treatment of childhood encopresis. Lancet 1991; 338: 523. 17. Achenbach TM: Manual for the Child Behavior Checklist 4-18, 1991 Profile. Burlington: University of Vermont 1991. 18. Arbeitsgruppe Deutsche Child Behavior Checklist. Deutsche Bearbeitung der Child Behavior Checklist (CBCL/4-18): Einführung und Anleitung zur Handauswertung, 2. Auflage mit deutschen Normen. Koeln: Arbeitsgruppe Kinder-, Jugend- und Familiendiagnostik 1999. 19. World Health Organization: The ICD-10 Classification of Mental and Behavioural Disorders. Di-
agnostic Criteria for Research. Geneva: World Health Organization 1993. 20. Butler RJ: Etablishment of working definitions in nocturnal enuresis. Arch Dis Child 1991; 66: 267. 21. van den Berg MM, Benninga MA and Di Lorenzo C: Epidemiology of childhood constipation: a systematic review. Am J Gastroenterol 2006; 101: 2401. 22. Pliszka S; AACAP Work Group on Quality Issues: Practice parameter for the assessment and treatment of children and adolescents with attentiondeficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2007; 46: 894. 23. Elia J, Takeda T, Deberardinis R et al: Nocturnal enuresis: a suggestive endophenotype marker for a subgroup on inattentive attention-deficit/hyperactivity disorder. J Pediatr 2009; 155: 239.
24. Järvelin MR, Moilanen I, Vikeväinen-Tervonen L et al: Life changes and protective capacities in enuretic and non-enuretic children. J Child Psychol Psychiatry 1990; 31: 763. 25. Järvelin MR, Vikeväinen-Tervonen L, Moilanen I et al: Enuresis in seven-year-old children. Acta Paediatr Scand 1988; 77: 148. 26. Wigal T, Greenhill L, Chuang S et al: Safety and tolerability of methylphenidate in preschool children with ADHD. J Am Acad Child Adolesc Psychiatry 2006; 45: 1294. 27. Van Hoecke E, Baeyens D, Vanden Bossche H et al: Early detection of psychological problems in a population of children with enuresis: construction and validation of the short screening instrument for psychological problems in enuresis. J Urol 2007; 178: 2611.