Rev. bras. psicoter. 2022; 24(2):43-59
Jacobsen GM, Prando ML, Motta GLCL, Kochhann R, Fonseca RP. Clusters de processamento executivo em crianças com diagnóstico de TDAH. Rev. bras. psicoter. 2022;24(2):43-59
Artigo Original
Clusters de processamento executivo em crianças com diagnóstico de TDAH
Executive processing clusters in school-age children with ADHD
Clusters de procesamiento ejecutivo en niños diagnosticados con TDAH
Geise Machado Jacobsen, Mirella Liberatore Prando, Gledis Lisiane Correa Luz Motta, Renata Kochhann, Rochele Paz Fonseca
Resumo
Abstract
Resumen
INTRODUCTION
Attention Deficit Hyperactivity Disorder (ADHD) is one of the most common neurodevelopmental conditions in childhood1-3. It is estimated that the prevalence of the condition among children varies from 5% to 7%4-5. The disorder is characterized by persistent symptoms of lack of attention and/or hyperactivity/ impulsivity above what is expected for the age bracket. These symptoms may yield losses in learning, affection, cognition, and social function of children1-3,6-7.
With respect to the neuropsychological profile of ADHD children, individuals with the disorder may present deficits in multiple neurocognitive processes and related cerebral systems. Also, different people can indicate different neuropsychological profiles, which only add to the complex and heterogenic characteristics of the condition8-9. Despite the diversity in cognitive profiles, deficits in executive functions (EF) components have been pointed as some of the main characteristics of ADHD10-12. Executive functions are a group of cognitive processes that work together to produce, execute, monitor, regulate, and readjust adequate conducts to attain complex goals13. According to Diamond14, these abilities can be comprehended through a model that includes the main components of cognitive flexibility, inhibition, and working memory, as well as the complex components of reasoning and problem solving.
In this sense, symptoms related to the disorder would arise from primary losses in executive components, such as inhibition or working memory, or even general executive difficulties. This proposal is based on evidence that pre-frontal lesions can produce symptoms associated with ADHD1,12,15-16. Barkley17, for example, proposes that the main ADHD characteristic is an inhibition deficit that harms other aspects of executive functioning.
According to Barkley17, inattention refers to the incapacity of maintaining attention on activities or tasks, remembering and following instructions or rules, and avoiding distractions. The author believes that ADHD's distinct inattention can be a consequence of executive problems, especially of working memory. On the same note, impulsivity is related to inhibition difficulties, involving losses in the ability to inhibit responses.
Overall, studies have found deficits in executive components such as cognitive flexibility, verbal fluency, inhibition, working memory, planning and vigilance, as well as difficulties in sustained attention3,12,16,18-19. Even though EF component deficits are prevalent in ADHD, they may not be present in all individuals who have the disorder10. Also, they are not specific to this condition and they are not necessary to reach diagnosis3.
Some studies have not detected differences between executive functions among the various presentations of ADHD20-21. Even so, there is evidence to support a distinct neuropsychological profile between presentations. Problems with learning and language (loss in comprehension, mathematics, and writing, for example) are more frequently associated with the predominantly inattentive type3,21-22. Executive deficits, on the other hand, are more closely related to the combined and hyperactive-impulsive types6,21. In summary, attention problems can generate more academic losses, while hyperactivity-impulsivity problems are more closely linked to behavioral issues. Working memory deficits are also associated with attention problems23.
Considering the neuropsychological profile heterogeneity among children with ADHD, especially with respect to EF, it is necessary to invest in understanding some key factors. Those include the specific aspects of executive components processing within the disorder, as well as which biological, individual, sociocultural, and clinical factors may explain the variability of the executive profiles. In order to investigate the executive abilities of abilities of children with ADHD, along with the variables that may be associated with their differences, cluster analyses may be performed.
However, studies about ADHD that have used this method are scarce. The majority of them have approached the differences between symptoms of inattentiveness and hyperactivity24-26 inattention, hyperactivity, and impulsivity, are expressed with various degrees of severity. The nature of the biological dysfunction sustaining each subtype (common or distinct. Only three researches have investigated differences in cognitive profiles between clusters. Bonafina, Newcorn, McKay, Koda and Halperin27 have analyzed subgroups of intellectual and reading abilities. Thaler and collaborators7 investigated subgroups of cognitive abilities in a sample of children with predominantly inattentive or combined ADHD types, based on WISC-IV. The first cluster presented reduced processing speed and higher incidence of diagnosis for the predominantly inattentive type, whereas the second cluster showed deficits in processing speed and working memory, as well as predominance of behavioral problems. Only one research has approached FE and ADHD clusters more specifically28. Three clusters were found: 1) difficulties in inhibitory control, 2) cognitive flexibility and processing speed problems, and 3) a subgroup with no executive losses. However, this investigation used only two EF measures: Stop Task, to evaluate inhibition, and Trail Making Task, to measure cognitive flexibility and processing speed. Therefore, studies that approach other EF evaluation paradigms are necessary, and they should include verbal measures as well as working memory examinations. That would allow the investigation of specific aspects of the different executive components and task models. Moreover, biological and sociocultural factors, as well as the intensity of inattention and hyperactivity symptoms, are yet to be studied and analyzed with respect to their impact on executive deficits that may be present in ADHD. In this context, the present study aimed 1) to identify subgroups within a sample of children with ADHD regarding the processing profile of the following executive components: cognitive flexibility, inhibition, and working memory; and 2) to identify whether clusters present differences concerning biological, clinical, and sociocultural factors.
METHOD
Procedures
The children were referred to participate in the research by two sources in Porto Alegre, Brazil: the Child Psychiatric Ambulatory team from a hospital, and health professionals from the private sector. Contact was made with parents and/or guardians to invite them to participate in the research. After the explanation of the study's goals, as well as details about ethical and data collection procedures, parents and/or guardians signed an informed consent form.
Participants were evaluated in a school clinic or in a private clinic in Porto Alegre. The children were individually assessed in two sessions that lasted around one hour each. With permission from the physician in charge, children who were under psychostimulant medication for ADHD had treatment suspended for a period of 24 or 48 hours before their assessment, depending on the type of medication.
Participants
Sixty-one children participated in this study. Selected individuals were between 6 and 12 years old (mean 9.18; standard deviation 1.56), from both genders (feminine: n=20; masculine: n=41), and enrolled in private (n=42) or public (n=19) schools. The following criteria were considered for exclusion: a) uncorrected sensory impairments (auditory and/or visual); b) history of neurological conditions; c) history of primary psychiatric disorders regarding ADHD; d) intelligence quotient (IQ) lower than 80, according to Wechsler Abbreviated Scale of Intelligence (WASI) (29); and e) participation in neuropsychological rehabilitation for EFs. From the initial sample of 80 participants, n=4 were excluded because they did not fulfill ADHD diagnostic criteria; n=13 were excluded because they presented IQ lower than 80, according to WASI; and n=2 were excluded due to history of neurological condition. Hence, there was a total of 19 exclusions.
Participants were diagnosed with ADHD by a neurologist or a psychiatrist from the referral sources. The diagnosis was confirmed by the researchers through a semi-structured clinical interview (Kiddie-Sads; 30) with the child and his/her parents and/or guardians, and complemented by data from the MTA-SNAP-IV questionnaire (31), filled by parents and/or guardians and by teachers of the participant. Children had either the inattentive (n=30) or the combined (n=31) presentation of ADHD. In the assessment made through the MTA-SNAP-IV questionnaire, on average, participants showed 6.36 (SD=1.47) inattentive symptoms with mean intensity of 16.11 (SD=3.86), and 4.16 (SD=2.81) hyperactivity symptoms with mean intensity of 11.83 (SD=6.21).
Among the 61 participants, n=43 showed writing and reading deficits in tasks of reading words and pseudowords to examine reading routes, and of writing under dictation to assess orthographic processing. Those tasks were used to track difficulties in these processes, due to the high level of comorbidity with learning disorders. Also, n=7 children presented comorbidity with other psychiatric disorders, being n=2 of them with diagnosis of anxiety; n=2 with depression; n=1 with bipolar disorder; n=1 with oppositional defiant disorder; and n=1 with enuresis. Comorbidities were informed by the neurologist or by the psychiatrist in charge of assisting the participant.
Instruments
1) Unconstrained Verbal Fluency (UVF), adapted for children by Jacobsen and collaborators (32) from the Montreal Communication Evaluation Battery33-34. Verbal fluency tasks assess executive and lexical-semantic processes, demanding attention, information update, capacity to: start the search, retrieve information from the lexicon, and organize a search strategy. They also require cognitive flexibility, inhibition, and working memory. During the UFV task, without phonemic-orthographic or semantic criteria, the child must recall as many words as possible during two minutes and thirty seconds, except for proper nouns (cities, countries, people, etc.) and numbers. Total switches (shifts between categories) are taken into consideration during task execution.
2) Narrative Discourse (ND), adapted for children by Prando and collaborators (35) from the Montreal Communication Evaluation Battery33-34. The instrument evaluates complex linguistic processing, as well as episodic and working memory. The task involves three steps: 1) partial retelling, in which the examiner reads a brief story, paragraph by paragraph, and, after each one, the child must retell it; 2) integral retelling, in which the examiner retells the complete story and, right after that, the participant must tell it with his/her own words; 3) text comprehension, in which the child is asked 11 questions about the story. The score of essential information retrieved during partial retelling (main elements of the story) is included in this study.
3) Wechsler Intelligence Scale for Children 3rd edition (WISC-III)36. Battery that allows the characterization of the neuropsychological profile from the assessment of various cognitive functions. The Digits subtest was applied, allowing the examination of selective auditory attention (direct order - DO) and of central executive system of working memory (inverse order - IO). In DO, the participant must repeat a sequence of numbers in the same order that he/she heard them. In IO, on the other hand, the participant must repeat them backwards. This study uses the following measures: total of correct responses in IO and discrepancy between the two parts of the test, which corresponds to the OD raw score minus the OI raw score.
4) Hayling Sentence Completion Test for Children (HSCT-C), adapted for Brazilian children by Siqueira and collaborators37, from the original version by Burgess and Shallice38. Task composed of two parts in which the participant must complete sentences whose last word is missing. Both parts of the instrument assess attention and processing speed. In the transition between parts A and B, cognitive flexibility ability may be observed. Specifically, part A is more closely related to the examination of verbal initiation and lexical search, whereas part B is more associated with the measurement of verbal inhibition and planning. In part A, the child must evoke, as quickly as possible, a word that coherently completes each of the ten sentences. Semantic and syntactic context leads to the activation of a coherent vocabulary. In part B, the examinee must complete the sentence with a word that is not related to the semantic and syntactic context, that is, he/she must inhibit the dominant word. This study includes scores for execution time (latency to respond to sentences), total number of mistakes in part B (words that have semantic association with the sentence), and execution time in part B minus execution time in part A.
Data analysis
Data were analyzed using SPSS 17.0 software for Windows, with a significance level of p≤0.05. Scores from tasks that assess the executive components of cognitive flexibility, inhibition, and central executive system of working memory were converted into Z scores, considering normative data from each instrument. From the Z scores, an EF general compound score, as well as a specific compound score for each executive component, was calculated, as shown in Figure 1. The general compound score includes all scores provided by each executive component. A hierarchical cluster analysis was conducted, using EF general compound score as the classification criterion. Given that three executive components were examined and that Roberts and collaborators (28) identified three groups in their study, three clusters were requested. Differences among clusters with respect to the following nominal variables were verified through a Chi-Square test: presentation of the disorder (combined or inattentive), difficulties in reading and writing (absence or presence), parental level of education (high or low), occurrence of deficits (absence or presence), gender (feminine or masculine), and type of school (private or public). Differences regarding age were examined using One-Way ANOVA. Because differences in age were coterminous and associations between different scores could occur, MANCOVA was conducted. In that analysis, age was controlled in order to verify differences between clusters with respect to compound scores, raw scores from EF tasks, and frequency/intensity of ADHD symptoms measured by MTA-SNAP-IV questionnaire.
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