Central Nervous System Processing of Emotions in Children with Fecal Incontinence and Constipation
A Replication Study
Abstract
Abstract.Objective: Fecal incontinence and constipation are common disorders in childhood. The enteric nervous system and the central nervous system are highly interactive along the brain-gut axis. The interaction is mainly afferent. These afferent pathways include centers that are involved in the central nervous processing of emotions as the mid/posterior insula and the anterior cingulate cortex. A previous study revealed altered processing of emotions in children with fecal incontinence. The present study replicates these results. Methods: In order to analyze the processing of emotions, we compared the event-related potentials of 25 children with fecal incontinence and constipation to those of 15 control children during the presentation of positive, negative, and neutral pictures. Results: Children with fecal incontinence and constipation showed altered processing of emotions, especially in the parietal and central cortical regions. Conclusions: The main study results of the previous study were replicated, increasing the certainty and validity of the findings.
Zusammenfassung.Fragestellung: Stuhlinkontinenz mit Obstipation ist eine häufige Erkrankung im Kindesalter. Das enterische Nervensystem (ENS) und das zentrale Nervensystem (ZNS) sind entlang der Darm-Hirn-Achse hoch vernetzt, mit vorwiegend Afferenzen vom ENS zum ZNS. Die Verbindungen umfassen Hirnzentren, die in die zentrale Emotionsverarbeitung involviert sind, wie die Insula und der anterior cinguläre Cortex. Eine vorherige Studie fand eine veränderte Emotionsverarbeitung bei Kindern mit Stuhlinkontinenz. Das Ziel der vorliegenden Studie war es, diese Befunde zu replizieren. Methodik: Bei 25 Kindern mit Stuhlinkontinenz und Obstipation sowie 15 Kontrollkindern wurde die Emotionsverarbeitung untersucht, indem ereigniskorrelierte Potenziale während der Präsentation von positivem, negativem und neutralem Bildmaterial gemessen wurden. Ergebnisse: Kinder mit Stuhlinkontinenz und Obstipation zeigten Veränderungen in der Emotionsverarbeitung, vor allem in parietalen und zentralen kortikalen Regionen. Schlussfolgerungen: Die wichtigsten Ergebnisse bezüglich einer veränderten Emotionsverarbeitung bei Kindern mit Stuhlinkontinenz und Obstipation konnten repliziert werden. Dies erhöht die Validität der Befunde.
Introduction
Fecal incontinence (FI), defined as the passage of stool in inappropriate places after organic causes have been ruled out (World Health Organization (WHO), 1993), is a common disorder in childhood. In an epidemiological study, 1.4 % of 7-year-old children soiled once a week or more, and 5.4 % soiled less than once a week (Joinson, Heron, Butler, von Gontard, & the ALSPAC Study Team, 2006). FI is often associated with constipation. The Rome-III classification differentiates between functional incontinence with or without FI and nonretentive FI (Rasquin et al., 2006).
The enteric nervous system is an independent nervous system of the gut which is similar to the central nervous system (CNS). The interaction along the brain-gut axis is mainly afferent with 90 % afferents from the gut to the CNS and only 10 % efferents. The afferent pathways include centers that are involved in the central nervous processing of emotions, such as the mid/posterior insula and the anterior cingulate cortex (Mayer, Naliboff, & Craig, 2006).
In a first study, Becker et al. (2011) showed altered CNS processing of emotions in children with FI with more intense responses in event-related potentials for different emotional stimuli over frontal, central, and parietal regions compared to continent control children.
The present study replicates results of this previous study (Becker et al., 2011) assessing CNS processing of emotions in a more homogeneous group, namely, in children with FI and constipation. We tested the hypothesis that children with FI and constipation show altered responses to emotional stimuli, indicating a disturbance of the brain-gut axis in these children.
Methods
A group of 25 children aged 5–11 years (mean age = 8.1 years; SD = 1.9) with FI and constipation were recruited from a special outpatient clinic for incontinence at the Department of Child and Adolescent Psychiatry, Saarland University Hospital, Germany. As a control group, 15 age- and sex-matched children (age range: 6–12 years, mean age = 9.2 years, SD = 1.8) were recruited from local sports clubs and by newspaper ads. The study was approved by the local ethics committee.
FI was diagnosed according to ICD-10-criteria (WHO, 1993) and constipation according to clinical symptoms and sonography examination according to Rome-III criteria (Rasquin et al., 2006). Psychological symptoms were measured using the Child Behavior Checklist (CBCL/4–18) (Achenbach, 1991), and child psychiatric diagnoses were assessed by a structured, standardized psychiatric interview (Kinder-DIPS) according to ICD-10-criteria (Schneider, Margraf, & Unnewehr, 1995). Intelligence quotient (IQ) was measured with a one-dimensional intelligence test (Coloured Progressive Matrices (CPM) or Standardized Progressive Matrices (SPM) (Raven, 1998; Raven, Raven, & Court, 2006). Additionally, a full child psychiatric assessment and a physical examination including sonography of the rectum were performed on every child.
The study design to assess event-related potentials was parallelized to the design of previous studies with children with FI (Becker et al., 2011) and children with nocturnal enuresis (NE) (Equit, Becker, El Khatib, Rubly, Becker, & von Gontard, 2014).
We presented 160 negative, neutral, and positive pictures from the standardized International Picture System (Lang, Bradley & Cuthbert, 1999). Additionally, 40 photographs of stool were presented. The pictures were presented as an oddball paradigm with standard, novel, and target pictures in three blocks in randomized order. The 40 target pictures consisted of neutral pictures rotated by 10 degrees. To sustain attention, participants were instructed to press a button after each target picture.
The event-related potentials (ERP) were recorded with the BrainVision Recorder 1.03.0003 (Brain Products GmbH). The methods of ERP assessment are described in detail in Becker et al. (2011) and Equit et al. (2014).
The descriptive statistics, Student t-tests for independent samples, Welch tests (if variance-homogeneity was not given), and c2-tests were calculated to compare the groups regarding sex, age, IQ, and psychological comorbidities. The mean activity of event-related potentials in the time intervals of 250–450 ms, 450–650 ms, and 650–850 ms was calculated. The following regions of interest (ROI) were defined: frontal (F3, Fz, F4), central (C3, Cz, C4), and parietal (P3, Pz, P4). The hypothesis was tested with repeated-measurement analyses of variance (ANOVAS). The effects were specified with uncorrected one-way ANOVAS. Violations of sphericity were adjusted with the Greenhouse-Geisser formula. A p < .05 was considered to be statistically significant.
Results
Children with FI and constipation did not differ from control children regarding age and sex, but they did differ significantly regarding IQ, with higher IQ among control children (see Table 1). In addition, children with FI had significantly higher T-values regarding externalizing and internalizing symptoms as well as higher rates of child psychiatric diagnoses (especially ADHD, oppositional defiant disorder, and NE/daytime urinary incontinence, Table 1).
In the analysis of the CNS processing of emotions, the repeated measures ANOVA revealed a main effect for group (F(1, 36) = 5.7, p = .022) over all time intervals, positions, and stimuli, showing a different reaction in children with FI and constipation compared to healthy controls. In order to specify the effect, we analyzed each time interval (250–450 ms, 450–650 ms, and 650–850 ms). The topographic map of the event-related potentials during the time interval 650–850 ms of children with FI and controls are shown in Figure 1. There was a significant main effect for the between-subject factor group (children with FI vs. controls) (F(1, 36) = 4.8, p = .035). Planned pairwise univariate analyses revealed significant differences between children with FI and controls for positive stimuli in the regions central (F(1, 36) = 5.9, p = .02) and parietal (F(1, 36) = 7.8, p = .008) with more positive grand averages in children with FI (central: X = 0.10 (SD = 7.33); parietal: X = 3.92 (SD = 8.19)) compared to controls (central: X = –5.47 (SD = 7.16); parietal: X = –3.48 (SD = 7.36)) (see Figure 2).
No significant main effects were found for the time intervals 250–450 ms and 450–650 ms.
Discussion
The present study succeeded in replicating the main results of our first study (Becker et al., 2011): Children with FI and constipation show more psychological symptoms and child psychiatric disorders as well as different CNS responses to emotional stimuli than do healthy controls.
In contrast to the former findings, however, patients in the present study had significantly different responses to positive stimuli at 650–850 ms interval (central and parietal), whereas in the former study, differences were found in the time intervals 250–450 ms and 450–650 ms over all ROIs. One explanation of these differences may lie in the different patient groups, since only patients with FI and constipation were included. Becker et al. (2011) also found differences in responses between FI and constipation and nonretentive FI, especially in central and parietal ROIs, which agrees with the current findings. These results indicate that the processing of emotions is altered especially in the parietal and central cortical region in children with FI and constipation.
One could speculate that children with FI and constipation have specific dysfunctions of higher CNS activity involving the processing of emotions, due perhaps to prolonged colon transit times and the chronic retention of stools in the rectum and the associated increased afferent activity to the CNS (Benninga, Voskuijl, Akkerhuis, Taminiau, & Buller, 2004).
Several previous studies showed a strong association between functional gastrointestinal disorders, FI and/or constipation, and psychological stress (e. g., Devanarayana & Rajindrajith, 2009). On the one hand, stress-induced psychological disturbances can emerge as results of the gastrointestinal disorder such as FI and disappear with successful treatment (Benninga et al., 2004). On the other hand, psychological stress may contribute to increased pelvic floor muscle tension (Whitehead, Wald, Diamant, Enck, Pemberton, & Rao, 1999) and correlate with rectal mucosal blood flow, indicating an influence on the gut function via efferent pathways (Emmanuel, Mason, & Kamm, 2001). The present study also turned up this association with psychological factors. Children with FI and constipation were significantly more affected by internalizing and externalizing symptoms and psychological disorders such as ADHD oppositional defiant disorder or NE/daytime urinary incontinence.
These comorbid psychological symptoms or disorders could be seen as a mediator between FI/constipation and altered CNS emotion processing. A previous study revealed more intense CNS emotion processing in children with NE and ADHD (Equit et al., 2014). Future research should compare children with FI and constipation with and without psychological symptoms as well as with and without NE/daytime urinary incontinence. Also, future studies should consider including a control group matched according to IQ and rates of psychological symptoms. A larger sample size could also serve to reveal different processing in other ROIs, which could not be detected in the present study because of the large variance in the grand averages.
Additionally, it would be interesting to compare CNS emotion processing in children with FI and constipation before and after treatment would, whether successful treatment normalizes emotion processing.
Overall, the measurement of ERPs has a good resolution over time. However, in order to obtain more information and to specify topographical regions of the CNS processes involved, structural and functional imaging studies with higher spatial resolution are needed in future research.
Conclusions
The reproducibility of study results is a defining feature of science. Nevertheless, direct replication studies are rarely conducted and/or published (Open Science Collaboration, 2012). The fact that we were able to replicate the main study results of our previous study (Becker et al., 2011) increases the certainty and validity of those findings.
Conflicts of interests: No conflicts of interest exist.
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