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Attention deficit hyperactivity disorder (ADHD) symptoms, comorbid psychopathology, behaviour problems and gastrointestinal symptoms in children and adolescents with autism spectrum disorder

Published online by Cambridge University Press:  11 May 2021

Geraldine Leader*
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Roisín Moore
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
June L. Chen
Affiliation:
Department of Special Education, Faculty of Education, East China Normal University, Shanghai, China
Aoife Caher
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Sophia Arndt
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Leanne Maher
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Katie Naughton
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Reanna Clune
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
Arlene Mannion
Affiliation:
Irish Centre for Autism and Neurodevelopmental Research (ICAN), School of Psychology, National University of Ireland, Galway, Ireland
*
*Address for correspondence: Geraldine Leader, Ph.D., Irish Centre for Autism and Neurodevelopmental Research, School of Psychology, National University of Ireland, Galway, Ireland. (Email: [email protected])
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Abstract

Objectives:

The study aims to investigate attention deficit hyperactivity disorder (ADHD) symptoms, gastrointestinal (GI) symptoms, comorbid psychopathology and behaviour problems in children and adolescents with autism spectrum disorder (ASD).

Methods:

Parents of 147 children and adolescents with ASD aged 6–18 years completed the Conners 3 Parent-Short Form, Gastrointestinal Symptom Inventory, Behavior Problems Inventory-Short Form and Autism Spectrum Disorder-Comorbid for Children.

Results:

Fifty-six per cent of children and adolescents had a comorbid diagnosis of ADHD, yet over 70% presented with clinically significant ADHD symptoms. Forty per cent of participants received a diagnosis of ADHD before ASD and 25.6% received a diagnosis of ASD first. Relationships were found between ADHD symptoms and comorbid psychopathology, GI symptoms, and behaviour problems.

Conclusions:

The outcomes suggest that ADHD is being underestimated as a comorbid disorder of ASD. This may have implications on treatment and interventions for children and adolescents who have a diagnosis of both ASD and ADHD.

Type
Original Research
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of The College of Psychiatrists of Ireland

Introduction

Autism spectrum disorder

Autism spectrum disorder (ASD) is a complex behavioural disorder characterised by social deficits, communication difficulties, stereotyped or repetitive behaviours and interests and cognitive delays according to the DSM-5 (American Psychiatric Association, 2013). The Center for Disease Control and Prevention has found that 1 in 54 children is diagnosed with ASD (Maenner et al. Reference Maenner, Shaw, Baio, Washington, Patrick and DiRienzo2020). The most recent data on the prevalence of ASD in Ireland were reported in a study (Boilson et al. Reference Boilson, Staines, Ramirez, Posada and Sweeney2016) which determined that 1.5% of children in Ireland have a diagnosis of ASD. Research conducted by the United Kingdom Department of Health reported that 4.2% of children in Northern Ireland have a diagnosis of ASD (Rodgers & McCluney, Reference Rodgers and McCluney2020). It was previously thought that the male-to-female ratio with ASD was 4:1, but a recent study by Loomes et al. (Reference Loomes, Hull and Mandy2017) determined that this statistic is closer to 3:1. ASD is usually identified in children by the age of 2 years when delays in language and social interactions begin to become noticeable (Lord et al. Reference Lord, Risi, DiLavore, Shulman, Thurm and Pickles2006).

Attention deficit hyperactivity disorder (ADHD)

Attention deficit hyperactivity disorder (ADHD) is a disorder that co-occurs with ASD (Mannion et al. Reference Mannion, Brahm and Leader2014). ADHD is associated with behaviour problems including inattention, hyperactivity and impulsivity. According to the DSM-5 (American Psychiatric Association, 2013), 5% of children in the general population have ADHD. In order to be diagnosed according to the DSM-5, a person must exhibit at least six symptoms from the categories of either or both inattention/hyperactivity and impulsivity (American Psychiatric Association, 2013). In Ireland, it has been found that less than 1% of children have received a formal diagnosis of ADHD (Williams et al. Reference Williams, Greene, Doyle, Harris, Layte, McCoy, McCrory, Murray, Nixon, O’Dowd, O’Moore, Quail, Smyth, Swords and Thornton2009; Adamis et al. Reference Adamis, Tatlow-Golden, Gavin and McNicholas2019). ADHD has been found to have a negative effect on occupational status and social interactions in people diagnosed with the disorder (Mannuzza et al. Reference Mannuzza, Klein, Bessler and Malloy1993; Mannuzza & Klein, Reference Mannuzza and Klein2000; Barkley, Reference Barkley2002).

Comorbid psychopathology in ASD

Comorbid psychopathology describes the presence of at least two forms of psychopathology within one individual (Matson & González, Reference Matson and González2007; Matson & Nebel-Schwalm, Reference Matson and Nebel-Schwalm2007). It is important that the primary diagnosis is asserted, so that future treatment and correct prioritisation of intervention goals occur (Matson & Nebel-Schwalm, Reference Matson and Nebel-Schwalm2007). Comorbid conditions in ASD and other developmental disorders include sleep problems, epilepsy, toileting problems, stimulus over-selectivity and behaviour problems (Devlin et al. Reference Devlin, Healy, Leader and Reed2008; Mannion & Leader, Reference Mannion and Leader2014 a, Reference Mannion and Leader2014 b; Kelly et al. Reference Kelly, Leader and Reed2015; Newman et al. Reference Newman, Leader, Chen and Mannion2015; Leader & Mannion, Reference Leader, Mannion and Matson2016 a; Francis et al. Reference Francis, Mannion and Leader2017).

Several studies have been conducted to examine the effect of comorbidity in individuals with ASD. Mannion et al. (Reference Mannion, Leader and Healy2013) found that 46.1% of children and adolescents diagnosed with ASD had a comorbid disorder. This rose to 78% when an intellectual disability (ID) was included. Furthermore, the researchers found that 18% of these children and adolescents had a comorbid diagnosis of ADHD. Thomas et al. (Reference Thomas, Lycett, Papadopoulos, Sciberras and Rinehart2018) found that out of a sample of 392 children with ADHD, 93 participants had a comorbid diagnosis of ASD, whereas 299 participants had ADHD alone. Ashwood et al. (Reference Ashwood, Tye, Azadi, Cartwright, Asherson and Bolton2015) determined that in a sample of 86 children, 38 participants had a comorbid diagnosis of ADHD and ASD, whereas 17 had ASD alone and 31 had ADHD alone.

ASD and ADHD

In the DSM-IV-TR (American Psychiatric Association, 2000), an ASD diagnosis did not allow for a comorbid diagnosis with certain disorders. Examples of these disorders were ADHD, stereotyped movement disorder and psychiatric conditions such as schizophrenia and anxiety states (Wing et al. Reference Wing, Gould and Gillberg2010). In the area of ASD, the DSM-5 (American Psychiatric Association, 2013) has allowed for dual diagnosis between ASD and ADHD. Recent research has found that symptoms of ADHD occur in children and adolescents with ASD without a comorbid diagnosis. May et al. (Reference May, Cornish and Rinehart2012) found that children with ASD had higher scores of ADHD symptoms compared to typically developing children (TD). Additionally, within the ASD group, young boys had higher levels of impulsivity and hyperactivity compared to girls and older children.

Other disorders such as dyspraxia frequently co-occur with ASD and ADHD as their impairments in motor skills commonly overlap. For example, research investigating ADHD have found that 50% of ADHD cases also have motor problems severe enough to be diagnosed with dyspraxia (Piek et al. Reference Piek, Pitcher and Hay1999; Pitcher et al. Reference Pitcher, Piek and Hay2003). Further, children initially diagnosed with dyspraxia have been found to also meet moderate to severe diagnosis for ADHD (Kadesjö & Gillberg, Reference Kadesjö and Gillberg1999). Significant motor impairments such as grip selection, fine and gross motor abilities and the production of gestures are evident as overlapping across individuals diagnosed with ASD and dyspraxia (Dewey et al. Reference Dewey, Cantell and Crawford2007; van Swieten et al. Reference van Swieten, van Bergen, Williams, Wilson, Plumb, Kent and Mon-Williams2010). Investigating comorbid disorders associated with ASD such as ADHD has crucial implications for treatment and diagnosis. Treatments available for individuals with ADHD have been shown to have positive effects (De Crescenzo et al. Reference De Crescenzo, Cortese, Adamo and Janiri2017).

Gastrointestinal symptoms

Gastrointestinal (GI) symptoms describe problems affecting the GI tract of an individual, leading to abnormalities such as constipation, diarrhoea or abdominal pain (Leader & Mannion, Reference Leader, Mannion and Matson2016 b). Children with ASD are more likely to present with GI symptoms than typically developing children and special needs children (Chandler et al. Reference Chandler, Carcani-Rathwell, Charman, Pickles, Loucas, Meldrum, Simonoff, Sullivan and Baird2013). The most common GI symptoms affecting individuals with ASD are constipation and abdominal pain with or without diarrhoea (Buie et al. Reference Buie, Campbell, Fuchs, Furuta, Levy and Vande Water2010). Nausea and bloating are also common symptoms in children with ASD (Mannion & Leader, Reference Mannion and Leader2013, Reference Mannion and Leader2016). Chandler et al. (Reference Chandler, Carcani-Rathwell, Charman, Pickles, Loucas, Meldrum, Simonoff, Sullivan and Baird2013) showed that 46.5% of children with ASD had at least one GI symptom in the past compared to 21.8% of TD children and 29.2% of special needs children. Mannion et al. (Reference Mannion, Leader and Healy2013) determined that 79.3% of children and adolescents with ASD had presented with at least one GI problem in the past 3 months. Additionally, the researchers found a relationship between GI symptoms and comorbid psychopathology, such as conduct, tantrum, avoidant and worry/depressed behaviours in children and adolescents with ASD. Further studies have also found links between language regression (Valicenti-McDermott et al. Reference Valicenti-McDermott, McVicar, Cohen, Wershil and Shinnar2008) and behavioural aetiologies for GI symptoms (Ibrahim et al. Reference Ibrahim, Voigt, Katusic, Weaver and Barbaresi2009) in children with ASD. Williams et al. (Reference Williams, Leader, Mannion and Chen2015) also examined the relationship between anxiety and GI symptoms and found that higher levels of anxiety are associated with higher levels of GI symptoms. Consistently, Mazurek et al. (Reference Mazurek, Vasa, Kalb, Kanne, Rosenberg, Keefer, Murray, Freedman and Lowery2013) found in a study that participants who reported nausea and constipation symptoms had higher levels of anxiety than those without GI symptoms.

GI symptoms have also been linked to ADHD. In a cohort study by McKeown et al. (Reference McKeown, Hisle-Gorman, Eide, Gorman and Nylund2013), it was found that children with ADHD had a higher rate of both constipation (4.1% in children with ADHD compared to 1.5% without) and faecal incontinence (0.9% in children with ADHD compared to 0.15% without) than children without ADHD.

Behaviour problems

Challenging behaviour is a well-documented, recurrent issue in the literature. Challenging behaviours are mainly defined as behaviours which are not socially acceptable, physically dangerous and those that negatively influence education (Matson et al. Reference Matson, Mahan, Hess, Fodstad and Neal2010; Jang et al. Reference Jang, Dixon, Tarbox and Granpeesheh2011). Hutchins & Prelock (Reference Hutchins and Prelock2014) reported that recent prevalence estimates of challenging behaviours in individuals with ASD/ID range from 35.8% to 64.3% with most studies reporting that more than half of these individuals engage in more than one challenging behaviour. A comorbid diagnosis with ASD can amplify the effects of challenging behaviour (Matson et al. Reference Matson, Mahan, Fodstad, Worley, Neal and Sipes2011). This can increase the severity of the primary disorder (Yerys et al. Reference Yerys, Wallace, Sokoloff, Shook, James and Kenworthy2009; Sprenger et al. Reference Sprenger, Bühler, Poustka, Bach, Heinzel-Gutenbrunner, Kamp-Becker and Bachmann2013; Rao & Landa, Reference Rao and Landa2013).

Maskey et al. (Reference Maskey, Warnell, Parr, Le Couteur and McConachie2013) found that half of the children with ASD in the study presented with at least 4 of 10 common behaviour problems. Behaviours presented consisted of sleep problems, toileting, hyperactivity, temper, aggression, self-injury, reluctance to separate from parent, anxiety, eating problems and sensory issues. The study is consistent with past studies such as Leyfer et al. (Reference Leyfer, Folstein, Bacalman, Davis, Dinh, Morgan, Tager-Flusberg and Lainhart2006) and Simonoff et al. (Reference Simonoff, Pickles, Charman, Chandler, Loucas and Baird2008). Behaviour problems can cause increased issues in areas unrelated to the behaviours themselves. It has been found that greater levels of behaviour problems can be associated with lower IQ and expressive/receptive language in children with ASD (Dominick et al. Reference Dominick, Davis, Lainhart, Tager-Flusberg and Folstein2007).

A comorbid diagnosis of ADHD and ASD increases impairment in challenging behaviour (Jang et al. Reference Jang, Dixon, Tarbox and Granpeesheh2011). Goldin et al. (Reference Goldin, Matson, Tureck, Cervantes and Jang2013) investigated the impact a comorbid diagnosis of ADHD and ASD can have on tantrum behaviours. In this study, the comorbid group was found to be significantly higher in tantrum behaviours than the other two groups (ASD only and ADHD only). Comorbid symptoms targeted by the Autism Spectrum Disorder-Comorbidity for Children (ASD-CC) (Matson & González, Reference Matson and González2007) was highest in the ADHD and ASD comorbid group. Konst et al. (Reference Konst, Matson and Turygin2013) found that children with ASD had a higher rate of tantrum behaviours than the ADHD group. The ASD and ADHD group presented with even higher rates of tantrum behaviour compared to the other two groups.

Current study

The present study aims to assess the impact of ADHD on children and adolescents with ASD. Additionally, the relationship between ADHD symptoms and challenging behaviour, comorbid psychopathology, and GI symptoms will be examined. The aim is to better understand whether children and adolescents with both ASD and ADHD symptoms are at an increased risk of challenging behaviour, comorbid psychopathology and GI symptoms. A hypothesis of this study is that children and adolescents with ASD without a diagnosis of ADHD will still exhibit ADHD symptoms.

Method

Participants

The sample for this study was 147 children and adolescents aged 6 to 17 years with a diagnosis of ASD in accordance with DSM-IV-TR criteria (American Psychiatric Association, 2000). Diagnoses were provided by a licensed psychologist or paediatrician independent of the study. The participants received their diagnosis as a result of the formal diagnostic protocol which employs multiple diagnostic measures. Caregiver information on professional diagnosis, diagnostic setting/organisation and professional(s) who made the diagnosis was obtained. Eighty-one per cent of children and adolescents included in the study were male (n = 119) and 19% were female (n = 28). The mean age for this study was 10.09 years (SD = 3.21). Nearly, half of all participants (44.9%; n = 66) had an ID. Of those diagnosed with an ID, 16.7% (n = 30) had a mild ID, 17.8% (n = 32) had a moderate ID, while 4.4% of participants (n = 8) had a severe ID.

Informants and procedure

Informants were parents of children and adolescents with ASD. Rating scales were completed by parents independently according to the instructions which were printed on the top of each questionnaire. Parents were recruited through schools, ASD service providers and parent support groups. If parents wished to participate in the study, they were provided with a participant information form and a consent form to complete. Once consent was obtained, the informants were provided with the battery of questionnaires to complete in their own time.

Measures

Demographic information questionnaire

Parents were asked to complete a self-constructed demographic information questionnaire which inquired about age and gender of the child. Parents were also asked about diagnosis of ASD, ADHD, ID (and severity), anxiety disorders, other comorbid disorders and at what age the child received their diagnoses.

Conners 3-Parent (Short Form)

The Conners 3-Parent (Short Form) (Conners, Reference Conners2008a) was used to assess the comorbid symptoms of ADHD. The scale is a 43-item parent-rated scale which asks parents to report on the previous month of the child’s behaviour to screen for ADHD symptoms. Inattention, hyperactivity/impulsivity, learning problems, executive functioning, aggression and peer relations were the norms assessed on the scale. The Conners 3 has been extensively researched and developed over a 4-year period and has been found to be reliable and valid (Izzo et al. Reference Izzo, Donati, Novello, Maschietto and Primi2019). Internal consistency coefficients range between .77 and .97, Cronbach’s alpha ranges between .71 and .98, and interrater reliability lies between .7 and .94 (Conners, Reference Conners2008b). Conners 3 has been tested for factorial, construct validity and predictive reliability. These reliability and validity accounts origin from a normative sample of 3,400 children from Canada and the United States (Conners, Reference Conners2008b). Cut-off scores for clinically elevated scores were set at a t-score of 65. However, an upper limit of 70 on the t-score can also be applied according to the Conners 3 Manual as very elevated (Conners, Reference Conners2008b).

Gastrointestinal Symptom Inventory

The Gastrointestinal Symptom Inventory (Autism Treatment Network, 2005) was used to assess GI symptoms. The scale consisted of a 35-item questionnaire which was based on experience of symptoms in the past 3 months, allowing assessment of presence and absence of different symptoms. The questionnaire allows branching of specific symptomatology, that is, bowel movements, constipations, etc. The Gastrointestinal Symptom Inventory was formed from previous questionnaires and clinical symptom assessment (Autism Treatment Network, 2005). This tool has not yet been validated. However, previous literature has used this scale (Mazurek et al. Reference Mazurek, Vasa, Kalb, Kanne, Rosenberg, Keefer, Murray, Freedman and Lowery2013; Leader et al. Reference Leader, Francis, Mannion and Chen2018).

Behavior Problems Inventory (BPI-S)

The Behavior Problems Inventory-Short Form (BPI-S) (Rojahn et al. Reference Rojahn, Rowe, Sharber, Hastings, Matson, Didden, Kroes and Dumont2012b) scale consisted of 30 items to assess challenging behaviours in terms of self-injurious behaviour (item 1–9), aggressive/destructive behaviours (item 10–18) and stereotyped behaviour (item 19–30). The scale assesses both frequency (monthly, weekly, daily and hourly) and severity of problem (mild, moderate and severity). The short form correlates with the BPI-01 (r = 0.96 to 0.99) and held sensitivity at 0.92 to 0.99 (Rojahn et al. Reference Rojahn, Rowe, Sharber, Hastings, Matson, Didden, Kroes and Dumont2012a). Internal consistency for both the frequency and severity scales on the BPI-S was reported to be 0.70 to 0.89 (Rojahn et al. Reference Rojahn, Rowe, Sharber, Hastings, Matson, Didden, Kroes and Dumont2012b). Convergent validity, discriminate validity and factorial validity are all robust in the BPI-S (Rojahn et al. Reference Rojahn, Rowe, Sharber, Hastings, Matson, Didden, Kroes and Dumont2012b).

Autism Spectrum Disorder-Comorbidity for Children (ASD-CC)

The ASD-CC (Matson & González, Reference Matson and González2007) assesses comorbid psychopathology in children and adolescents with ASD. The scale consisted of 39 items which were marked on a 3-point Likert scale. It consists of seven subscales: Tantrum Behavior, Repetitive Behavior, Worry/Depressed, Avoidant Behavior, Under Eating, Over Eating and Conduct. Matson et al. (Reference Matson, LoVullo, Rivet and Boisjoli2009) showed that the ASD-CC has validity with construct validity being established for Tantrum Behavior, Repetitive Behavior, Worry/Depressed, Conduct, Over Eating and to a lesser extent, Under-eating. Matson & Wilkins (Reference Matson and Wilkins2008) determined interrater, test–retest and internal reliabilities for the ASD-CC showing reliability for all items in the scale.

Results

Analyses

Descriptive statistics including means, standard deviations and frequencies were calculated for the variables. Clinically elevated t-scores from the Conners T-scores in each of its subscales were generated. A one-way ANOVA was conducted to assess the effect of ADHD diagnosis on the Conners subscales. Two ANOVAs were conducted to examine the relationship between ADHD symptoms and ID severity and anxiety. Correlations were conducted to assess the effects of the Conners subscales on the BPI-S, Gastrointestinal Symptom Inventory and the ASD-CC. Two independent t-tests were conducted to compare learning problems in those with GI symptoms compared to those with no GI symptoms.

Descriptive statistics

Respondents were asked if their child had a diagnosis of ADHD, ID and/or an anxiety disorder. A diagnosis of ADHD was present in 56.5% (n = 83) of participants. Table 1 provides a summary of demographic information. Additionally, ADHD diagnosis was evaluated through diagnosis dates, and it was found that 40.2% of participants had a diagnosis of ADHD before being diagnosed with ASD. It was also found that 25.6% were diagnosed with ASD first and 34.1% were diagnosed with ASD and ADHD at the same time.

Table 1. Demographic information

M, mean; SD, standard deviation.

Mean differences between the group with ADHD and the group without ADHD were examined in terms of GI symptoms (as measured by the Gastrointestinal Symptom Inventory), behaviour problems (as measured by the BPI-S) and comorbid psychopathology (as measured by the ASD-CC). It was found that 75.5% of participants presented with between one and six GI symptoms. In relation to the groups with ADHD and without ADHD, there were differences between types of GI symptoms experienced. The group with ADHD had higher mean scores for experiencing bloating and constipation.

Mean scores for behaviour problems based on the BPIS (self-injurious behaviour frequency and severity, aggressive/destructive behaviour frequency and severity, and stereotyped behaviour frequency) were higher in the group without ADHD across all domains.

Mean scores for comorbid psychopathology assessed by the ASD-CC showed higher means scores across tantrum, undereating and conduct behaviours in participants with a diagnosis of ADHD compared to those without ADHD. Very little difference in mean scores was observed between the two groups based on overeating, repetitive and worry behaviour domains.

Clinically elevated T-scores from the Conners T-scores were assessed in each of the subscales; hyperactivity, inattention, learning problems, executive functioning, aggression and peer relations. Over seventy percent of the total population scored above 65, indicating clinically elevated scores on the Conners Scale. Ninety-one percent reported clinically elevated scores on hyperactivity, 91% for inattention, 71% for learning problems, 80% for executive functioning, 65% for aggression, and 65% for peer relations.

Inferential statistics

A one-way ANOVA was conducted to assess the effect of ADHD diagnosis on Conners subscales. A difference between groups was found in the subscale inattention (F(1,145) = 8.18, p < .005). Descriptively, inattention had a mean score of 82.39 in the ADHD diagnosis group, compared to 77.14 without an ADHD diagnosis group. All other areas were similar in mean scores and did not show significant differences between the groups.

Two one-way between subjects ANOVA was conducted to examine the relationships between the presence of an anxiety disorder and the severity of an ID on the Conners subscales. Results found that the presence of an anxiety disorder (F(1,145) = 8.12, p < .005) and ID severity was significant in one subscale, learning problems (F(3,143) = 17.90, p < .000). Post hoc comparisons using the Tukey HSD test indicated that the mean score for no ID (M = 66.21, SD = 12.26) was significantly different than the mild ID (M = 75.30, SD = 10.51), moderate ID (M = 81.59, SD = 8.43) and severe ID (M = 81.00, SD = 8.19) conditions.

A correlation was conducted to assess Conners subscales effect on the BPI-S. Aggression significantly correlated with all subscores of the BPI-S. Inattention, hyperactivity/impulsivity, learning problems, executive functioning, aggression and peer relations also significantly correlated with some areas of the BPI-S as can be seen in Table 2.

Table 2. Correlation between Conner’s subscales and BPI-S

IN, inattention; HYP, hyperactivity/impulsivity; LP, learning problems; EF, executive functioning; A, aggression; PR, peer relations.

p < 0.05*, p < 0.01**.

A correlation between the scores of ASD-CC and Conners subscales was performed. Tantrum behaviour significantly correlated with all subscales of the Conners scale. A summary of the results can be seen in Table 3.

Table 3. Correlations between ASD-CC and Conners subscales

p < 0.05*, p < 0.01**

Significant correlations were also found between total GI symptoms and the Conners subscales. Table 4 presents a summary of the results.

Table 4. Correlations between total GSI and Conners subscales

p < 0.05*, p < 0.01**.

A series of independent t-tests were conducted to compare learning problems in children with GI symptoms to those without GI symptoms. Results revealed a significant difference in learning problems between individuals who experienced bloating compared to those who did not experience bloating (t (145) = −2.95, p = .004). Children and adolescents experiencing bloating had more learning problems (M = 77.34, SD = 12.22) than children and adolescents who did not experience bloating (M = 70.43, SD = 12.52). There was a significant difference in learning problems between the presence of other GI symptoms (other than constipation, diarrhoea, abdominal pain, bloating and nausea) compared to those who had no other GI symptoms (t (145) = −2.42, p = .017). Children and adolescents who presented with other GI symptoms (M = 76.39, SD = 11.33) had significantly more learning problems than children and adolescents without other GI symptoms (M = 70.71, SD = 12.97).

Discussion

One of the central aims of this study was to determine the frequency of both ADHD diagnosis and symptoms of ADHD in children and adolescents with ASD. The study found that children and adolescents with ASD without a diagnosis of ADHD still exhibited symptoms of ADHD. Over half of the participants (56.5%) included in this study had a comorbid diagnosis of ADHD with ASD. However, over 70% of participants presented with clinically significant ADHD symptoms. The study examined the relationship between ADHD symptoms and GI symptoms, behaviour problems and comorbid psychopathology.

Relationships were found between inattention and comorbid psychopathology. Specifically, relationships were found between inattention and tantrum, repetitive, conduct, and overeating behaviours. Inattention is defined by poor attention and difficulty concentrating (Conners, Reference Conners2008b). The results indicate that tantrum, repetitive, conduct and overeating behaviours are contingent on the child’s inability to focus. Relationships were also found between inattention and behaviour problems. Specifically, relationships were found between inattention and the severity and frequency of aggressive/destructive behaviours and the frequency of stereotyped behaviour. These findings are supported by the Individuals with Disabilities Act (2014) which found that children with ADHD inattention type are at a higher risk for both learning disabilities and emotional disturbances (Conners, Reference Conners2008b).

A relationship was found between hyperactivity and behaviour problems. The results indicate that children and adolescents with ASD who exhibit hyperactivity display more aggressive/destructive behaviour, stereotyped behaviour and self-injurious behaviour. Significant relationships were found between hyperactivity and all the ASD-CC subscales measuring comorbid psychopathology. Hyperactivity is associated with restlessness and impulsivity (Conners, Reference Conners2008b) and according to the Individuals with Disabilities Act (2014), this puts children with high scores on this scale at risk of emotional disturbances.

A relationship was found between executive functioning scores and comorbid psychopathology, specifically tantrum, repetitive, worry/depressed, avoidant, undereating and conduct behaviours. Executive functioning was associated with behaviour problems such as the frequency and severity of aggressive/destructive behaviour and the frequency of stereotyped behaviours. Executive functioning is associated with poor organisation and difficulty beginning projects (Conners, Reference Conners2008b). This is line with previous research which found that ADHD can have a negative effect on occupational status and social interactions, which may result from poor executive functioning (Mannuzza et al. Reference Mannuzza, Klein, Bessler and Malloy1993; Mannuzza & Klein, Reference Mannuzza and Klein2000; Barkley, Reference Barkley2002).

Relationships were found between the Conners subscale of aggression and comorbid psychopathology. Specifically, relationships were found between aggression and tantrum behaviour, repetitive behaviour, worry/depressed behaviour and conduct behaviour. Additionally, aggression was found to correlate significantly with of the BPI-S subscales based on the frequency and severity of self-injurious, aggressive/destructive and stereotyped behaviours. The correlation between aggression on both scales indicate that the scales showed reliability and were consistent in measurement of behaviours. The results of the study show that challenging behaviour is influenced by comorbid disorders, as demonstrated in the past studies (Matson et al. Reference Matson, Mahan, Fodstad, Worley, Neal and Sipes2011; Goldin et al. Reference Goldin, Matson, Tureck, Cervantes and Jang2013; Konst et al. Reference Konst, Matson and Turygin2013). Aggression, like hyperactivity, has an effect on behaviours that can be challenging to treat (Matson & Nebel-Schwalm, Reference Matson and Nebel-Schwalm2007).

Based on the Conners scale, peer relations relate to having difficulty with friendships, poor social skills, or seems to be unaccepted by groups (Conners, Reference Conners2008b). This scale showed the highest level of difficulty in the group with 97.3% of children and adolescents with ASD showing clinically elevated scores. This may demonstrate the relationship between ASD and difficulties in peer relations. This could be related more to the diagnosis of ASD rather than the diagnosis of ADHD, as ASD is characterised by issues with social communication according to the DSM-5 (American Psychiatric Association, 2013). Relationships were found between peer relations and comorbid psychopathology, specifically tantrum, worry/depressed and avoidant behaviours. Peer relations was also associated with the severity of aggressive/destructive behaviours based on the BPI-S.

A significant relationship was found between GI symptoms and learning problems. Further analysis revealed that learning problems were more prevalent in children and adolescents who experienced bloating and other GI symptoms compared to those who did not. Learning problems are understood as difficulties with learning or understanding material that may indicate a specific learning disability in children with ADHD (Conners, Reference Conners2008b). Chandler et al. (Reference Chandler, Carcani-Rathwell, Charman, Pickles, Loucas, Meldrum, Simonoff, Sullivan and Baird2013) found no link between intellectual ability and GI symptoms. Ibrahim et al. (Reference Ibrahim, Voigt, Katusic, Weaver and Barbaresi2009) found that GI symptoms could be linked to behavioural aetiologies, particularly constipation and feeding issues/selectivity, and it may be these behaviours influencing significance in the learning problems subscale.

Learning problems also had a significant relationship with comorbid psychopathology, correlating with all subscales on the ASD-CC. Results also indicated that children and adolescents diagnosed with an anxiety disorder in the study showed more learning problems than those without an anxiety disorder. This finding indicates that comorbid psychopathology in children and adolescents with ASD and ADHD is linked to increased learning problems. Results also suggested that a mild, moderate or severe ID were linked to more learning problems in children with ASD and ADHD.

There are multiple strengths to this study. Unlike other studies which focused on ADHD and ASD comorbidity (May et al. Reference May, Cornish and Rinehart2012; Goldin et al. Reference Goldin, Matson, Tureck, Cervantes and Jang2013; Konst et al. Reference Konst, Matson and Turygin2013), this study did not use an ADHD-only group and TD children and adolescents as controls. However, by looking at an ASD-only group to study ADHD comorbidity, it was possible to determine the effect the subscales had on these children and adolescents. A limitation was that data collection through parental report. Parents were the only caregivers that were asked to respond to the questionnaire; however, a child’s behaviours may be different in various settings. For example, some studies have found that parent and teacher ratings have low agreement in ADHD symptoms (Antrop et al. Reference Antrop, Roeyers, Oosterlaan and Van Oost2002; Murray et al. Reference Murray, Kollins, Hardy, Abikoff, Swanson, Cunningham, Vitiello, Riddle, Davis, Greenhill, McCracken, McGough, Posner, Skrobala, Wigal, Wigal, Ghuman and Chuang2007). Future research investigating the relationship between parent and teacher ratings with children and adolescents with a comorbid diagnosis of ASD and ADHD is recommended. This would further develop understanding of these disorders. A strength of this study was the construct validity between the scales used. Behaviours like aggression in the Conners correlated with their counter parts in the BPI-S.

Future research examining the relationship between ASD and ADHD diagnosis is needed. In this study, the age at which diagnosis was made were examined. Forty per cent of participants received a diagnosis of ADHD before ASD and 25.6% received a diagnosis of ASD first. Previous diagnosis may indicate primary diagnosis; however, future studies may find that symptomology may be affected by primary and secondary diagnosis of ADHD. Finally, research examining comorbidity in ASD and ADHD in adulthood would add to the understanding of the research area. As the DSM-5 has only begun to allow for a comorbid diagnosis between these two disorders, individuals who were previously diagnosed under the DSM-IV-TR could have symptoms of ADHD without a diagnosis.

This study has implications for the diagnosis of ADHD in an ASD population. Nearly, all children and adolescents in the study were found to have clinically elevated scores in the Conners subscales, and further studies may investigate if parents were aware of an ADHD diagnosis or whether parents had referred to medical professionals to investigated comorbidity. Additionally, due to the relative new allowance of ADHD and ASD in the same individual from the DSM-5 (American Psychiatric Association, 2000), there is potential for children and adolescents with a comorbid diagnosis to avail of better treatment and assessment to deal with the increased problems that arise from a comorbid diagnosis.

In conclusion, this was the first study to examine the differences in GI symptoms, comorbid psychopathology and behaviour problems between children and adolescents with an ADHD diagnosis and ADHD symptoms and those without a diagnosis and symptoms in children and adolescents with ASD. Furthermore, by investigating these differences, it was possible to distinguish the different effects ADHD symptoms had on GI symptoms, comorbid psychopathology and behaviour problems. The results found that ADHD symptoms increase behaviour problems and comorbidities that were related to ASD. Future research should examine these relationships in more detail to form better treatment and interventions for children and adolescents with a comorbid diagnosis of ADHD and ASD.

Compliance with Ethical Standards

Conflicts of interest

None.

Ethical standards

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committee on human experimentation with the Helsinki Declaration of 1975, as revised in 2008. Informed consent was obtained from all individual participants included in the study. The study protocol was approved by the ethics committee of the participating institution.

Financial support

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

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Figure 0

Table 1. Demographic information

Figure 1

Table 2. Correlation between Conner’s subscales and BPI-S

Figure 2

Table 3. Correlations between ASD-CC and Conners subscales

Figure 3

Table 4. Correlations between total GSI and Conners subscales