EEG-Messung von Emotionsverarbeitung bei Kindern mit funktioneller Harninkontinenz
Abstract
Abstract.Objective: Daytime urinary incontinence (DUI) is common in childhood. The aim of the study was to neurophysiologically analyse the central emotion processing in children with DUI. Method: In 20 children with DUI (mean age 8.1 years, 55 % male) and 20 controls (mean age 9.1 years, 75 % male) visual event-related potentials (ERPs) were recorded after presenting emotionally valent (80 neutral, 40 positive, and 40 negative) pictures from the International Affective Picture System (IAPS) as an oddball-paradigm. All children received a full organic and psychiatric assessment. Results: Children with DUI did not differ significantly from controls regarding responses to emotional pictures in the frontal, central, and parietal regions and in the time intervals 250–450 ms, 450–650 ms, and 650–850 ms after stimulus onset. The patient group had more psychological symptoms and psychiatric comorbidities than the control group. Conclusions: EEG responses to emotional stimuli are not altered in children with DUI. Central emotion processing does not play a major role in DUI. Further research, including a larger sample size, a more homogeneous patient group (regarding subtype of DUI) or brain imaging techniques, could reveal more about the central processing in DUI.
Zusammenfassung.Fragestellung: Die funktionelle Harninkontinenz (FHI) ist eine häufige Erkrankung im Kindesalter. Das Ziel dieser Studie war es, die zentrale Emotionsverarbeitung bei Kindern mit funktioneller Harninkontinenz (FHI) mit neurophysiologischen Methoden zu untersuchen. Methodik: Bei 20 Kindern mit FHI (Durchschnittsalter 8,1 Jahre, 55 % männlich) und 20 Kontrollen (Durchschnittsalter 9,1 Jahre, 75 % männlich) wurden visuelle, späte ereigniskorrelierte Potenziale in einem Oddball-Paradigma mit emotional gefärbten Bildern (40 positive, 40 negative und 80 neutrale) aus dem International Affective Picture System (IAPS) abgeleitet. Zusätzlich erfolgte eine umfassende Diagnostik psychiatrischer Symptome und Ausscheidungsstörungen. Ergebnisse: Die Patientengruppe zeigte im Vergleich zu der Kontrollgruppe keine signifikant intensiveren Reaktionen auf emotionale Stimuli. Dabei wurden die ROIs frontal, zentral und parietal und die Zeitintervalle 250–450 ms, 450–650 ms und 650–850 ms nach Reizdarbietung betrachtet. Die Patientengruppe hatte insgesamt mehr psychische Symptome sowie komorbide psychiatrische Störungen. Schlussfolgerungen: Kinder mit FHI zeigen keine signifikant intensiveren Reaktionen auf emotionale Stimuli im EEG. Dies bedeutet, dass die zentralnervöse Emotionsverarbeitung bei FHI eine geringere Rolle spielt. Möglicherweise könnten Untersuchungen mit größeren Stichproben und homogeneren Gruppen (bzgl. Subtyp der FHI) und bildgebende Verfahren die Rolle des zentralen Nervensystems bei der FHI besser aufklären.
Introduction
Daytime urinary incontinence (DUI) is diagnosed in children after the age of five years, when wetting occurs at least once a month and organic causes can be excluded (Austin et al., 2015). Next to nocturnal enuresis and faecal incontinence, DUI is a common disorder in children, with a prevalence of about 2–3 % in seven-year olds (Franco, Austin, Bauer, Von Gontard, & Homsy, 2015). The most common subtypes of DUI in children are urge incontinence (symptoms: urgency, high frequency, low voiding volumes), voiding postponement (postponing micturition, low frequency, holding manoeuvres, large voiding volumes), and dysfunctional voiding (straining while voiding, interrupted stream, residual urine) (Austin et al., 2015).
During micturition, not only bladder and brainstem, but also higher cerebral centres are involved. Fowler and Griffiths integrated functional brain imaging studies into a model of cerebral pathways of micturition (Fowler & Griffiths, 2010). During bladder filling and emptying, several brain structures, such as the periaqueductal gray (PAG), hypothalamus, thalamus, anterior cingulate cortex (ACC), insula and the prefrontal cortex as well as pathways between the structures are involved (Fowler & Griffiths, 2010). Some of these structures, such as the prefrontal cortex and the ACC, are also involved in emotion perception and regulation processes (Phillips, Ladouceur, & Drevets, 2008). Therefore, it can be hypothesized that emotion processing is disturbed in persons with uncontrolled bladder functions.
Altered CNS processing of emotions measured with event-related potentials has already been demonstrated in children with different subtypes of incontinence (Becker, Rubly, El Khatib, Becker, & von Gontard, 2011; Equit et al., 2014). Compared to healthy control children, children with nocturnal enuresis had more intense responses to emotionally valent pictures in the frontal region (Equit et al., 2014); and children with fecal incontinence showed more intense responses in the frontal, central, and parietal regions (Becker et al., 2011). There exist no data on altered emotion processing in children with DUI.
The aim of this study was to close this gap and to assess event-related potentials (ERPs) after presentation of emotional stimuli in children with DUI. It is hypothesized that children with DUI have more intense responses to emotional stimuli compared to a healthy control group.
Methods
Twenty children with DUI (5–13 years) were recruited from a specialized incontinence clinic at the Department of Child and Adolescent Psychiatry, Saarland University Hospital, Germany. The control group included 20 children who were recruited through newspaper ads and local sports clubs and were matched according to age and gender.
DUI was diagnosed according to the ICCS guidelines (Austin et al., 2015) after a complete incontinence examination, including history, 48h-bladder diary, uroflowmetry, sonography, and a physical examination. Additionally, a full child psychiatric assessment was conducted in every patient including the Child Behavior Checklist (CBCL/4-18) (Achenbach, 1991) to measure psychological symptoms, a standardised parental interview (Kinder-DIPS) to diagnose psychiatric disorders according to ICD-10-criteria (Schneider, Margraf, & Unnewehr, 1995), and a one-dimensional intelligence test (Coloured Progressive Matrices (CPM) or Standardized Progressive Matrices (SPM) (J. Raven, Raven, & Court, 2006; J. C. Raven, 1998).
Event-related potentials (ERP) were assessed in the same way as described previously (Becker et al., 2011; Equit et al., 2014). A total of 160 negative, neutral, and positive pictures from the standardised International Affective Picture System (IAPS) (Lang, Bradley, & Cuthbert, 1999) were presented as an oddball-paradigm with standard, novel, and target pictures randomised in three blocks. Forty neutral pictures (= target pictures) were rotated by 10 degrees and participants were instructed to press a button immediately after presentation to maintain attention. ERPs were recorded with the BrainVision Recorder 1.03.0003 (Brain Products GmbH). The mean activities of ERPs were calculated in three time intervals (250–450 ms, 450–650 ms, and 650–850 ms) in three regions of interest (ROI): frontal (F3, Fz, F4), central (C3, Cz, C4), and parietal (P3, Pz, P4). Repeated measures ANOVAs with between-factor groups (patients vs. controls) and within-factors ROI (frontal, central, parietal) and stimulus (negative, positive, neutral) were calculated. Age and gender were included as covariates. A p < 0.05 was considered as statistically significant. Effect sizes are reported as f-values (f = .10 (small effect), f = .25 (medium effect), f = .40 (large effect)).
Descriptive statistics were analysed with Student’s t-tests and c2-tests.
Results
Descriptive data are outlined in Table 1. Children with DUI did not differ from control children regarding age, gender, and IQ. Significant differences between groups were found regarding mean T-values of the externalizing, internalizing, and total scales of the CBCL. Comorbid psychiatric diagnoses were more frequent in patients than in controls (45.0 % vs. 5.0 %).
While analysing the CNS processing of emotions, the repeated measures ANOVA showed no main effect for group (F(1, 36) = 0.13; p = .722) over all time intervals, positions, and stimuli. Examining the three time intervals (250–450 ms, 450–650 ms, and 650–850 ms) separately, significant main effects for groups were neither found for the intervals 250–450 ms (F(1, 36) = 0.034; p = .854; f = .03), 450–650 ms (F(1, 36) = 0.002; p = .961; f = .01) nor for 650–850 ms (F(1, 36) = 0.911; p = .346; f = .16). The grand averages of both groups after stimuli onset over frontal, central, and parietal regions are shown in Figure 1, means and standard deviations (SD) are outlined in Table 2.
A post-hoc power analysis was calculated with the programme G*Power (Faul, Erdfelder, Lang, & Buchner, 2007) based on n = 40, α = .05, and medium effect sizes (f = .25) that were detected in the studies of Becker et al. (2011) and Equit et al. (2014). The calculated power can be estimated as .94 for the present study.
Discussion
This is the first study that assessed emotion processing in children with DUI compared to typically developing continent children. The results show no different responses to emotional stimuli in children with DUI and controls, neither in several ROIs (frontal, central, parietal) nor in different time intervals. These findings stand in contrast to results of former assessments in children with nocturnal enuresis or faecal incontinence (Becker et al., 2011; Equit et al., 2014).
The obvious conclusion is that there are no changes in emotion processing in children with DUI. In contrast to nocturnal enuresis, which is primarily caused by maturational deficits in the brain stem in non-organic or functional DUI, dysfunction of the bladder and lower urinary tract play a greater etiological role (Franco et al., 2015). Also, DUI comprises a heterogeneous group of disorders. Voiding postponement represents a learned behaviour, in which genetic or neurological factors do not play a major role (von Gontard, Niemczyk, Wagner, & Equit, 2016). Urge incontinence (or overactive bladder) is caused by spontaneous detrusor contractions, which are insufficiently inhibited by the central nervous system (CNS) (Franco et al., 2015). As the present patient group consists primarily of children with voiding postponement, one explanation for the negative results could be that CNS processes are not primarily involved and therefore emotion processing in these children is less impaired than e. g. in children with pure nocturnal enuresis.
Regarding the effect sizes, a small effect (f = .16) was reported for the late time interval (650–850 ms), which did not reach significance. This can be explained by the statistical power, which is sufficient enough for the detection of a medium effect but probably not for a small effect. The power could be raised, if a larger sample group was to be examined.
For future research projects, it would be interesting to compare emotion processing in different subtypes of DUI. Unfortunately, the subgroups in the present sample (six with urge incontinence, 14 with voiding postponement) are too small to conduct further analyses.
Psychological comorbidity was higher in children with DUI than in controls. This is in accordance with other findings of psychopathology in children with DUI, which are about twice as high in population-based studies (Joinson, Heron, & Von Gontard, 2006). In the present sample, comorbidity rates were even higher (45 % vs. 5 % in controls), including externalizing (15 %) but also internalizing disorders (20 %). In previous studies, conducted with the same methodology, patient groups with ADHD were included (Becker et al., 2011; Equit et al., 2014). Children with ADHD differed significantly from children with faecal incontinence, but not from healthy controls (Becker et al., 2011). The authors concluded that ADHD as a comorbid disorder does not explain the differences in emotion processing between children with faecal incontinence and controls. Otherwise, children with nocturnal enuresis and ADHD had more intense emotion processing than controls and children with nocturnal enuresis alone (Equit et al., 2014). In the present study, responses to emotional stimuli do not differ between groups, although psychological comorbidities (including ADHD) are more frequent. Therefore, one can conclude that additional psychiatric disorders, especially ADHD, have an effect on emotion processing in nocturnal enuresis, but not in faecal incontinence or DUI. Altered processing in several networks of the CNS and brain structures (e. g. prefrontal cortex regions) are discussed in individuals with both ADHD and nocturnal enuresis (von Gontard & Equit, 2015), which could also affect emotion regulation processes. As only two children with DUI had ADHD in this study, the effect of ADHD in emotion processing with DUI cannot be analysed reliably. Therefore, it would be revealing to assess children with DUI with and without comorbid ADHD in future studies.
The high rate of emotional disorders (20 %) in the present sample shows that especially anxiety disorders are present in children with DUI but not depressive disorders. Although former studies focused on externalizing disorders (ADHD), future research should also include anxiety problems in children with incontinence, as they could affect emotional processing as well. In a larger sample, subtle differences might be discernible, such as diverging responses in children with voiding postponement vs. urge incontinence, or in children with subclinical anxiety problems vs. clinical anxiety problems.
Strengths and Limitations
One strength of the present study is the measurement of emotion processing by objective electrophysiological method with a good resolution over time and a well-known paradigm with standardized picture material. Further, the patient group was diagnosed according to ICCS guidelines and psychiatric comorbidity was assessed with standardized instruments (including a structured parental interview, IQ test, and a validated questionnaire).
As a limitation, the small and heterogeneous patient group has to be considered. A larger sample would allow more detailed statistical analyses and a comparison between subtypes of DUI. Finally, the EEG measurement has a low spatial resolution; therefore, exact localisation of the event-related potentials activity in cortical or subcortical structures is difficult.
Conclusion
The present study is the first assessing emotion processing in children with DUI. The results show that children with DUI have no altered EEG responses to emotional stimuli compared to continent children, despite higher rates of psychiatric disorders. This stands in contrast to results in children with nocturnal enuresis or faecal incontinence. Further replication studies with larger samples should be conducted to increase the validity of the findings.
Ethical Approval and Informed Consent
All procedures performed were in accordance with the standards of the local ethics committee and with the 1964 Helsinki declaration and its later amendments. Informed consent was obtained from all individual participants included in the study.
Abbreviations
ACC = Anterior cingulate cortex, ADHD = Attention-deficit/Hyperactivity Disorder, CBCL = Child Behavior Checklist, CNS = Central nervous system, DUI = Daytime urinary incontinence, ERP = Event-related potentials, ICCS = International Children’s Continence Society, PAG = Periaqueductal gray, ROI = Region of interest.
Conflicts of interests: None
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