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Speech-language pathology findings in Attention Deficit Hyperactivity Disorder: a systematic literature review

ABSTRACT

Purpose

To systematically review the scientific production on the relationship between Attention Deficit Hyperactivity Disorder (ADHD) and Speech-language Pathology and to methodologically analyze the observational studies on the theme.

Research strategies

Systematic review of the literature conducted at the databases Medical Literature Analysis and Retrieval System online (MEDLINE, USA), Literature of Latin America and the Caribbean Health Sciences (LILACS, Brazil) and Spanish Bibliographic Index of Health Sciences (IBECS, Spain) using the descriptors: “Language”, “Language Development”, “Attention Deficit Hyperactivity Disorder”, “ADHD” and “Auditory Perception”.

Selection criteria

Articles published between 2008 and 2013. Inclusion criteria: full articles published in national and international journals from 2008 to 2013. Exclusion criteria: articles not focused on the speech-language pathology alterations present in the attention deficit hyperactivity disorder.

Data analysis

The articles were read in full and the data were extracted for characterization of methodology and content.

Results

The 23 articles found were separated according to two themes: Speech-language Pathology and Attention Deficit Hyperactivity Disorder.

Conclusion

The study of the scientific production revealed that the alterations most commonly discussed were reading disorders and that there are few reports on the relationship between auditory processing and these disorders, as well as on the role of the speech-language pathologist in the evaluation and treatment of children with Attention Deficit Hyperactivity Disorder.

Keywords
Speech, Language and Hearing Sciences; Attention Deficit Disorder with Hyperactivity; Language; Auditory Perception; Child

RESUMO

Objetivo

revisar sistematicamente as produções científicas acerca das relações entre o Transtorno de Déficit de Atenção e Hiperatividade e a Fonoaudiologia e analisar, metodologicamente, os estudos observacionais sobre a temática.

Estratégia de pesquisa

trata-se de revisão sistemática de literatura, realizada nas bases de dados Medical Literature Analysis and Retrieval System on-line (MEDLINE, EUA), Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS, Brasil) e Indice Bibliográfico Español de Ciencias de la Salud (IBECS), na qual foram utilizados os descritores “Linguagem”, “Desenvolvimento da Linguagem”, “Transtorno do Déficit de Atenção com Hiperatividade”, “TDAH” e “Percepção Auditiva”.

Critérios de seleção

foram selecionados artigos publicados entre 2008 e 2013. Os critérios de inclusão foram: artigos completos, publicados em periódicos nacionais e internacionais, no período de 2008 a 2013. Como critério de exclusão, foram considerados os artigos que não apresentavam, como foco principal, as alterações fonoaudiológicas presentes no Transtorno de Déficit de Atenção e Hiperatividade.

Análise dos dados

foi realizada a leitura dos artigos na íntegra e a extração de dados para caracterização da metodologia e do conteúdo das pesquisas.

Resultados

foram encontrados 23 artigos, os quais foram separados de acordo com dois eixos temáticos, relacionados à Fonoaudiologia e ao Transtorno de Déficit de Atenção e Hiperatividade.

Conclusão

o estudo das produções científicas revelou que as alterações fonoaudiológicas mais abordadas foram os distúrbios de leitura e que há poucas publicações acerca da relação entre o processamento auditivo e o transtorno, bem como a respeito da atuação do fonoaudiólogo na avaliação e no tratamento de crianças com Transtorno de Déficit de Atenção e Hiperatividade.

Descritores
Fonoaudiologia; Transtorno do Déficit de Atenção com Hiperatividade; Linguagem; Percepção Auditiva; Criança

INTRODUCTION

Attention Deficit Hyperactivity Disorder (ADHD) is one of the most common mental conditions in children. It is often identified at school age, when the demand for attention and inhibition of behavior is greater. The main characteristics of ADHD are inattention, hyperactivity, and impulsivity, whose manifestations may be related to predominantly inattentive, predominantly hyperactive, or combined subtypes(11 APA: American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4th ed. Washington, DC; 2000.).

Among the difficulties observed in children with ADHD are those related to the phonological aspects of language and the learning of metalinguistic skills. Deficits in the relation between working memory and performance in activities affect the development of phonological awareness and may lead to difficulties in learning to read(22 Oliveira AM, Cardoso MH, Pinheiro FH, Germano GD, Capellini SA. Desempenho de escolares com dislexia e transtorno do déficit de atenção e hiperatividade nos processos de leitura. Rev Bras Crescimento Desenvolv. Hum. 2011;21(2):344-55.).

It is also worth mentioning the relation between ADHD and auditory processing disorder, which has been discussed in some studies(33 Borja A, Ponde M. P300: avaliação do potencial evocado cognitivo em crianças com e sem TDAH. Rev Ciênc Méd Biol. 2009;8(2):198-205.,44 Pereira VRC, Santos TMM, Feitosa MAG. Sinais comportamentais dos Transtornos do Déficit de Atenção com Hiperatividade e do Processamento Auditivo: a impressão de profissionais brasileiros. Audiol Communic Res. 2013;18(1):1-9. http://dx.doi.org/10.1590/S2317-64312013000100003.
http://dx.doi.org/10.1590/S2317-64312013...
). One of the studies that reported the impression of Brazilian professionals on this relationship(44 Pereira VRC, Santos TMM, Feitosa MAG. Sinais comportamentais dos Transtornos do Déficit de Atenção com Hiperatividade e do Processamento Auditivo: a impressão de profissionais brasileiros. Audiol Communic Res. 2013;18(1):1-9. http://dx.doi.org/10.1590/S2317-64312013000100003.
http://dx.doi.org/10.1590/S2317-64312013...
) shows that some behavioral signs are characteristic of ADHD, whereas others are characteristic of auditory processing disorders. This fact suggests that ADHD and auditory processing disorder possibly occur independently.

Note that the aforementioned characteristics can determine impairments in the learning process and cognitive-linguistic skills. Therefore, it is necessary to investigate the relationship between Speech-Language Pathology disorders and ADHD, as well as to analyze the instruments used to assess these changes.

PURPOSE

The aim of this study is to systematically review the scientific productions addressing the relationship between Attention Deficit Hyperactivity Disorder (ADHD) and Speech-language Pathology, as well as to methodologically analyze the observational studies on the theme.

SEARCH STRATEGY

This is a systematic review of the literature, based on national and international recommendations(55 Zina LG, Moimaz SAS. Odontologia baseada em evidência: etapas e métodos de uma revisão sistemática. Arq Odontol. 2012;48(3):188-99.,66 Braga R, Melo M. Como fazer uma Revisão Baseada na Evidência. Rev Portug de Medicina Geral e Familiar. 2009;25(6):660-6.), with the following guiding question: “What are the possible Speech-Language Pathology disorders observed in children with Attention Deficit Hyperactivity Disorder (ADHD)?”

After defining the guiding question, the review was prepared in two phases: the first phase comprised the identification of the theme, search for the topic in the literature, categorization and evaluation of the included studies, interpretation of the results, and synthesis of the knowledge evidenced in the articles analyzed, as proposed in the literature(77 Malta M, Cardoso LO, Bastos FI, Magnanini MMF, Silva CMFP. Iniciativa STROBE: subsídios para a comunicação de estudos observacionais. Rev Saude Publica. 2010;44(3):559-65. PMid:20549022. http://dx.doi.org/10.1590/S0034-89102010000300021.
http://dx.doi.org/10.1590/S0034-89102010...
); in the second phase, the articles that fit the evidence matrix were included in the study.

The literature search on the theme of interest was conducted at the electronic databases Medical Literature Analysis and Retrieval System on-line (MEDLINE, USA), Literature of Latin America and the Caribbean Health Sciences (LILACS, Brazil), and Spanish Bibliographic Index of Health Sciences (IBECS, Spain) from July 2013 to January 2014. Original and review articles in English, Portuguese, and Spanish published between 2008 and 2013 were surveyed. At completion of the searches in all databases, references in duplicate were deleted.

The following English, Spanish and Portuguese keywords, found in the trilingual and structured vocabulary Health Sciences Descriptors (DeCS), were used in the search: “Language”, “Language Development”, “Attention Deficit Hyperactivity Disorder”, “ADHD”, and “Auditory Perception”.

SELECTION CRITERIA

Original research articles, published in Portuguese, Spanish or English, indexed between January 2008 and December 2013 were included in this study.

According to the proposed criteria, the following types of publications were excluded from the study: articles that did not respond to the guiding question, articles addressing Attention Deficit Hyperactivity Disorder in adults, review articles, abstracts in congress proceedings, theses, and dissertations. Based on the classification of levels of scientific evidence, case study articles and expert opinions were excluded. Twenty-seven articles that fit the second evidence matrix were selected for this systematic review; of these, 22 analytical observational studies and one descriptive exploratory study were included and two case reports and two literature reviews were excluded.

DATA ANALYSIS

The articles selected in the first phase were critically analyzed and distributed according to two main themes, namely: 1) studies that used only the Speech-language Pathology assessment of ADHD; and 2) studies that used both Speech-language Pathology and Neuropsychology assessments of ADHD. After that, the observational studies were analyzed according to the propositions of the STROBE (STrengthening the Reporting of OBservational studies in Epidemiology) Statement(77 Malta M, Cardoso LO, Bastos FI, Magnanini MMF, Silva CMFP. Iniciativa STROBE: subsídios para a comunicação de estudos observacionais. Rev Saude Publica. 2010;44(3):559-65. PMid:20549022. http://dx.doi.org/10.1590/S0034-89102010000300021.
http://dx.doi.org/10.1590/S0034-89102010...
), which was developed by researchers from the fields of epidemiology, statistics, and scientific methodology and by editors of scientific journals in order to disseminate the guiding principles for the description of observational studies. The STROBE Statement is composed of 22 items related to information that should be present in the sections Title, Abstract, Introduction, Methodology, Results, and Discussion of articles. After analysis based on this information, the studies were classified as follows: compliant (C), partly compliant (PC), and non-compliant (NC). The studies classified as C and PC were grouped according to a final classification described in Chart 1.

Chart 1
Analysis of the observational studies according to compliance with the STROBE Statement

RESULTS

The initial search found 4121 references. According to established inclusion criteria - complete articles addressing the study theme within the area of interest of Speech-Language Pathology published in the last five years in national and international journals - 3727 papers were selected for analysis. After the reading of titles and abstracts, 144 articles were selected and read in full. Twenty-seven articles were found at the end of the present review: 21 cross-sectional, analytical, observational studies; one longitudinal, analytical, observational study; one descriptive, exploratory study; two case reports; two literature reviews. No experimental, analytical studies were found.

As previously mentioned, case reports and literature reviews were excluded from this review. Thus the final corpus consists of 23 articles, of which six are national publications and 17 are international publications (Figure 1). The articles were grouped according to theme axes and distributed in tables for presentation of results.

Figure 1
Diagram of the selection process of the studies

Tables 1 and 2 show the main characteristics of the articles that have focused respectively on 1) studies that used only the Speech-language Pathology assessment of ADHD and 2) studies that used both Speech-language Pathology and Neuropsychology assessments of ADHD.

Table 1
Description of the studies that used only the Speech-language pathology assessment of Attention Deficit Hyperactivity Disorder
Table 2
Description of the studies that used both Speech-language pathology and Neuropsychology assessments of Attention Deficit Hyperactivity Disorder

Analysis of the selected studies according to the proposed theme axes

Six articles were found within the first thematic axis - studies that used only the Speech-language Pathology assessment of ADHD(88 Abdo AGR, Murphy CFB, Schochat E. Habilidades auditivas em crianças com dislexia e transtorno do déficit de atenção e hiperatividade. Pró-Fono Revista de Atualização Científica. 2010;22(1):25-30. PMid:20339804. http://dx.doi.org/10.1590/S0104-56872010000100006.
http://dx.doi.org/10.1590/S0104-56872010...

9 Wiemes GRM, Kozlowski L, Mocellin M, Hamerschmidt R, Schuch LH. Cognitive evoked potentials and central auditory processing in children with reading and writing disorders. Braz J Otorhinolaryngol. 2012;78(3):91-7. http://dx.doi.org/10.1590/S1808-86942012000300016.
http://dx.doi.org/10.1590/S1808-86942012...

10 Lobo PAS, Lima LAM. Comparação do desempenho em leitura de palavras de crianças com e sem Transtorno de Déficit de Atenção/Hiperatividade. Rev. CEFAC. 2008;10(4):471-83. http://dx.doi.org/10.1590/S1516-18462008000400007.
http://dx.doi.org/10.1590/S1516-18462008...

11 Silva C, Cunha VLO, Capellini SA. Desempenho cognitivo-linguístico e em leitura de escolares com transtorno de déficit de atenção e hiperatividade. Rev Bras Crescimento Desenvolv Hum. 2011;21(3):849-58.

12 Gallo LA, Muñoz MCL, Contreras DCM, Albores DA. Vocabulario expresivo en una muestra de niños preescolares con trastornos psiquiátricos y un grupo con desarrollo típico. Rev Salud Mental. 2011;34(4):315-22.
-1313 Gallardo-Paúls B, Moreno-Campos P, Roca P, Pérez-Mantero JL. Complejidad sintáctica y textual en niños con transtorno por déficit de atención/hiperactividad. Rev Neurol. 2012;54(1):131-5.). One of these surveys(88 Abdo AGR, Murphy CFB, Schochat E. Habilidades auditivas em crianças com dislexia e transtorno do déficit de atenção e hiperatividade. Pró-Fono Revista de Atualização Científica. 2010;22(1):25-30. PMid:20339804. http://dx.doi.org/10.1590/S0104-56872010000100006.
http://dx.doi.org/10.1590/S0104-56872010...
) used the tests of Frequency Pattern and Dichotic Digits. Another study(99 Wiemes GRM, Kozlowski L, Mocellin M, Hamerschmidt R, Schuch LH. Cognitive evoked potentials and central auditory processing in children with reading and writing disorders. Braz J Otorhinolaryngol. 2012;78(3):91-7. http://dx.doi.org/10.1590/S1808-86942012000300016.
http://dx.doi.org/10.1590/S1808-86942012...
) used the Dichotic Speech test (Staggered Spondaic Words - SSW) and conducted the electrophysiological assessment by means of the Cognitive Evoked Potential (P300). The objective of the first study was to investigate the performance of children with dyslexia and Attention Deficit Hyperactivity Disorder through auditory processing behavioral tests. In the latter study, the aim was to identify if above the average of P300 latency values, in a group of individuals with Reading and Writing Disability, changes suggestive of Auditory Processing Disorder would also be found in the Staggered Spondaic Word (SSW) and Speech in Noise tests.

Although the study that used electrophysiological assessment, by means of the P300, did not include children with Attention Deficit Hyperactivity Disorder, the results found in the group with Reading and Writing Disability were similar to those presented by children with ADHD in a previous study(33 Borja A, Ponde M. P300: avaliação do potencial evocado cognitivo em crianças com e sem TDAH. Rev Ciênc Méd Biol. 2009;8(2):198-205.). These results refer to the finding of higher latencies and lower amplitudes of the P300, which may be related to a slow maturation of the central auditory pathways.

It is worth mentioning that in the studies that evaluated the performance of children with ADHD or with Reading and Writing Disability by auditory processing assessment tests(88 Abdo AGR, Murphy CFB, Schochat E. Habilidades auditivas em crianças com dislexia e transtorno do déficit de atenção e hiperatividade. Pró-Fono Revista de Atualização Científica. 2010;22(1):25-30. PMid:20339804. http://dx.doi.org/10.1590/S0104-56872010000100006.
http://dx.doi.org/10.1590/S0104-56872010...
,99 Wiemes GRM, Kozlowski L, Mocellin M, Hamerschmidt R, Schuch LH. Cognitive evoked potentials and central auditory processing in children with reading and writing disorders. Braz J Otorhinolaryngol. 2012;78(3):91-7. http://dx.doi.org/10.1590/S1808-86942012000300016.
http://dx.doi.org/10.1590/S1808-86942012...
), both groups presented unsatisfactory performance in the applied tests. In the case of the first study, which evaluated a group of children with ADHD, the low performance in the auditory processing tests may be related to attention and auditory processing abilities. The second study highlights that learning, reading and writing, and ADHD disorders, among others, should be considered as differential diagnoses, so that they are not confused with auditory processing disorders, although they may coexist. In this sense, there is a need for further studies that investigate the relationship between ADHD and auditory processing disorder.

With respect to reading, one of the studies(1010 Lobo PAS, Lima LAM. Comparação do desempenho em leitura de palavras de crianças com e sem Transtorno de Déficit de Atenção/Hiperatividade. Rev. CEFAC. 2008;10(4):471-83. http://dx.doi.org/10.1590/S1516-18462008000400007.
http://dx.doi.org/10.1590/S1516-18462008...
), whose objective was to determine whether children with and without ADHD presented differences in silent reading at the level of decoding of isolated words, reported that attention interfered both in the perception of the read item and in the adequacy of reading. The performance of the group of children with ADHD suggests total errors in the reading of pseudowords and a trend to more pronounced lexicalizations in activities that involve orthographic processing. These errors may be related to better performance in phonological processing tasks compared with visual processing tasks and to exclusively phonological reading, without lexical addressing.

In a study conducted in Brazil(1111 Silva C, Cunha VLO, Capellini SA. Desempenho cognitivo-linguístico e em leitura de escolares com transtorno de déficit de atenção e hiperatividade. Rev Bras Crescimento Desenvolv Hum. 2011;21(3):849-58.), the authors compared the cognitive-linguistic and reading performance of schoolchildren with ADHD with that of schoolchildren without complaints of behavioral and/or learning disorders; they observed that the difficulties presented by the students with ADHD can be attributed to the characteristics of hyperactivity, inattention, and disorganization, but not to a phonologically-based language disorder.

The relationship between expressive vocabulary and psychiatric disorders was investigated in an international study(1212 Gallo LA, Muñoz MCL, Contreras DCM, Albores DA. Vocabulario expresivo en una muestra de niños preescolares con trastornos psiquiátricos y un grupo con desarrollo típico. Rev Salud Mental. 2011;34(4):315-22.) that compared the lexicon of children with ADHD, Autism Spectrum Disorder (ASD), Asperger Syndrome (AS), and other psychiatric disorders. According to the authors, the children with a diagnosis of ASD presented smaller vocabulary than those of the other studied groups, followed by the group that presented other psychiatric disorders. The performance of the latter group was similar to that of children with typical language development. Performance in the vocabulary test was similar between the groups with ADHD and with AS. The authors also emphasized that there was statistical significance only between the ASD and ADHD groups, and they support that language delay in preschool children with ADHD indicates a need for better investigation of the diagnosis of ASD.

Another study conducted in Spain(1313 Gallardo-Paúls B, Moreno-Campos P, Roca P, Pérez-Mantero JL. Complejidad sintáctica y textual en niños con transtorno por déficit de atención/hiperactividad. Rev Neurol. 2012;54(1):131-5.), analyzed the syntax complexity of phrases and the use of verbal tenses by children and adolescents with and without ADHD. The results of this study showed that children with ADHD presented lower values for the levels of syntactic complexity, as well as in the use of subordination, compared with those of the control group. The authors highlight that differences in the verbal management of temporality, associated with grammar verb tenses, can be considered important features in the language of children and adolescents with ADHD.

Analysis of the second thematic axis, concerning studies that used both Speech-language Pathology and Neuropsychology assessments of ADHD, revealed 17 articles(1414 Raghubar K, Cirino P, Barnes M, Ewing-Cobbs L, Fletcher J, Fuchs L. Errors in multi-digit arithmetic and behavioral inattention in children with math difficulties. J Learn Disabil. 2009;42(4):356-71. PMid:19380494. http://dx.doi.org/10.1177/0022219409335211.
http://dx.doi.org/10.1177/00222194093352...

15 Cutting LE, Materek A, Cole CAS, Levine TM, Mahone EM. Effects of fluency, oral language, and executive function on reading comprehension performance. Ann Dyslexia. 2009;59(1):34-54. PMid:19396550. http://dx.doi.org/10.1007/s11881-009-0022-0.
http://dx.doi.org/10.1007/s11881-009-002...

16 Kibby MY, Kroese JM, Krebbs H, Hill CE, Hynd GW. The pars triangularis in dyslexia and ADHD: a comprehensive approach. Brain Lang. 2009;111(1):46-54. PMid:19356794. http://dx.doi.org/10.1016/j.bandl.2009.03.001.
http://dx.doi.org/10.1016/j.bandl.2009.0...

17 Silveira DC, Passos LMA, Santos PC, Chiappetta ALML. Avaliação da fluência verbal em crianças com transtorno da falta de atenção com hiperatividade: um estudo comparativo. Rev CEFAC. 2009;11(2):208-16.

18 Li JJ, Cutting LE, Ryan M, Zilioli M, Denckla MB, Mahone EM. Response variability in rapid automatized naming predicts reading comprehension. J Clin Exp Neuropsychol. 2009;31(7):877-88. PMid:19221923. http://dx.doi.org/10.1080/13803390802646973.
http://dx.doi.org/10.1080/13803390802646...

19 Kibby MY, Pavawalla SP, Fancher JB, Naillon AJ, Hynd GW. The relationship between cerebral hemisphere volume and receptive language functioning in dyslexia and Attention-Deficit/Hyperactivity Disorder. J Child Neurol. 2010;24(4):438-48. PMid:19211921. http://dx.doi.org/10.1177/0883073808324772.
http://dx.doi.org/10.1177/08830738083247...

20 Willcutt EG, Betjemann RS, McGrath LM, Chhabildas NA, Olson RK, DeFries JC, et al. Etiology and neuropsychology of comorbidity between RD and ADHD: the case for multiple-deficit models. Cortex. 2010;46(10):1345-61. PMid:20828676. http://dx.doi.org/10.1016/j.cortex.2010.06.009.
http://dx.doi.org/10.1016/j.cortex.2010....

21 Hart SA, Petrill SA, Willcutt E, Thompson LA, Schatschneider C, Deater-Deckard K, et al. Exploring how symptoms of attention-deficit/hyperactivity are related to reading and mathematics performance: general genes, general environments. Psychol Sci. 2010;21(11):1708-15. PMid:20966487. http://dx.doi.org/10.1177/0956797610386617.
http://dx.doi.org/10.1177/09567976103866...

22 Booth R, Happé F. “Hunting with a knife and . . . fork”: examining central coherence in autism, attention deficit/hyperactivity disorder, and typical development with a linguistic task. J Exp Child Psychol. 2010;107(4):377-93. PMid:20655060. http://dx.doi.org/10.1016/j.jecp.2010.06.003.
http://dx.doi.org/10.1016/j.jecp.2010.06...

23 Okuda PMM, Pinheiro FH, Germano GD, Padula NAMR, Lourencetti MD, Santos LCA, et al. Função motora fina, sensorial e perceptiva de escolares com transtorno do déficit de atenção com hiperatividade. J Soc Bras Fonoaudiol. 2011;23(4):351-7. PMid:22231056. http://dx.doi.org/10.1590/S2179-64912011000400010.
http://dx.doi.org/10.1590/S2179-64912011...

24 Londoño DMM, Cifuentes VV, Lubert CD. Caracterización neuropsicológica de una muestra de niños y niñas con tdah de la ciudad de Manizales. Biosalud. 2011;10(1):30-51.

25 Jacobson LA, Ryan M, Martin RB, Ewen J, Mostofsky SH, Denckla MB, et al. Working Memory Influences Processing Speed and Reading Fluency in ADHD. Child Neuropsychol. 2011;17(3):209-24. PMid:21287422. http://dx.doi.org/10.1080/09297049.2010.532204.
http://dx.doi.org/10.1080/09297049.2010....

26 Gooch D, Snowling M, Hulme C. Time perception, phonological skills and executive function in children with dyslexia and/or ADHD symptoms. J Child Psychol Psychiatry. 2011;52(2):195-203. PMid:20860755. http://dx.doi.org/10.1111/j.1469-7610.2010.02312.x.
http://dx.doi.org/10.1111/j.1469-7610.20...

27 Simos PG, Rezaie R, Fletcher JM, Juranek J, Passaro AD, Li Z, et al. Functional disruption of the brain mechanism for reading: effects of comorbidity and task difficulty among children with developmental learning problems. Neuropsychology. 2011;25(4):520-34. PMid:21574715. http://dx.doi.org/10.1037/a0022550.
http://dx.doi.org/10.1037/a0022550...

28 Greven CU, Rijsdijk FV, Asherson P, Plomin R. A longitudinal twin study on the association between ADHD symptoms and Reading. J Child Psychol Psychiatry. 2012;53(3):234-42. PMid:21819398. http://dx.doi.org/10.1111/j.1469-7610.2011.02445.x.
http://dx.doi.org/10.1111/j.1469-7610.20...

29 Rosenberg J, Pennington BF, Willcutt EG, Olson RK. Gene by environment interactions influencing Reading Disability (RD) and the inattentive symptom dimension of Attention Deficit/Hyperactivity Disorder (ADHD). J Child Psychol Psychiatry. 2012;53(3):243-51. PMid:21884522. http://dx.doi.org/10.1111/j.1469-7610.2011.02452.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
-3030 Birkett EE, Talcott JB. Interval timing in children: effects of auditory and visual pacing stimuli and relationships with reading and attention variables. PLoS One. 2012;7(8):e42820. PMid:22900054. http://dx.doi.org/10.1371/journal.pone.0042820.
http://dx.doi.org/10.1371/journal.pone.0...
), which assessed not only the Speech-language Pathology disorders observed in ADHD, but also the aspects related to neuropsychological performance, through specific tests and scales of evaluation of the disorder. Among the studies included in this theme axis, eight addressed reading difficulties(1515 Cutting LE, Materek A, Cole CAS, Levine TM, Mahone EM. Effects of fluency, oral language, and executive function on reading comprehension performance. Ann Dyslexia. 2009;59(1):34-54. PMid:19396550. http://dx.doi.org/10.1007/s11881-009-0022-0.
http://dx.doi.org/10.1007/s11881-009-002...
,1717 Silveira DC, Passos LMA, Santos PC, Chiappetta ALML. Avaliação da fluência verbal em crianças com transtorno da falta de atenção com hiperatividade: um estudo comparativo. Rev CEFAC. 2009;11(2):208-16.,1818 Li JJ, Cutting LE, Ryan M, Zilioli M, Denckla MB, Mahone EM. Response variability in rapid automatized naming predicts reading comprehension. J Clin Exp Neuropsychol. 2009;31(7):877-88. PMid:19221923. http://dx.doi.org/10.1080/13803390802646973.
http://dx.doi.org/10.1080/13803390802646...
,2020 Willcutt EG, Betjemann RS, McGrath LM, Chhabildas NA, Olson RK, DeFries JC, et al. Etiology and neuropsychology of comorbidity between RD and ADHD: the case for multiple-deficit models. Cortex. 2010;46(10):1345-61. PMid:20828676. http://dx.doi.org/10.1016/j.cortex.2010.06.009.
http://dx.doi.org/10.1016/j.cortex.2010....
,2525 Jacobson LA, Ryan M, Martin RB, Ewen J, Mostofsky SH, Denckla MB, et al. Working Memory Influences Processing Speed and Reading Fluency in ADHD. Child Neuropsychol. 2011;17(3):209-24. PMid:21287422. http://dx.doi.org/10.1080/09297049.2010.532204.
http://dx.doi.org/10.1080/09297049.2010....
,2828 Greven CU, Rijsdijk FV, Asherson P, Plomin R. A longitudinal twin study on the association between ADHD symptoms and Reading. J Child Psychol Psychiatry. 2012;53(3):234-42. PMid:21819398. http://dx.doi.org/10.1111/j.1469-7610.2011.02445.x.
http://dx.doi.org/10.1111/j.1469-7610.20...

29 Rosenberg J, Pennington BF, Willcutt EG, Olson RK. Gene by environment interactions influencing Reading Disability (RD) and the inattentive symptom dimension of Attention Deficit/Hyperactivity Disorder (ADHD). J Child Psychol Psychiatry. 2012;53(3):243-51. PMid:21884522. http://dx.doi.org/10.1111/j.1469-7610.2011.02452.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
-3030 Birkett EE, Talcott JB. Interval timing in children: effects of auditory and visual pacing stimuli and relationships with reading and attention variables. PLoS One. 2012;7(8):e42820. PMid:22900054. http://dx.doi.org/10.1371/journal.pone.0042820.
http://dx.doi.org/10.1371/journal.pone.0...
); two dealt with difficulties of math and reading(1414 Raghubar K, Cirino P, Barnes M, Ewing-Cobbs L, Fletcher J, Fuchs L. Errors in multi-digit arithmetic and behavioral inattention in children with math difficulties. J Learn Disabil. 2009;42(4):356-71. PMid:19380494. http://dx.doi.org/10.1177/0022219409335211.
http://dx.doi.org/10.1177/00222194093352...
,2121 Hart SA, Petrill SA, Willcutt E, Thompson LA, Schatschneider C, Deater-Deckard K, et al. Exploring how symptoms of attention-deficit/hyperactivity are related to reading and mathematics performance: general genes, general environments. Psychol Sci. 2010;21(11):1708-15. PMid:20966487. http://dx.doi.org/10.1177/0956797610386617.
http://dx.doi.org/10.1177/09567976103866...
); three had the relation between cerebral structures and the alterations of language as their main focus(1616 Kibby MY, Kroese JM, Krebbs H, Hill CE, Hynd GW. The pars triangularis in dyslexia and ADHD: a comprehensive approach. Brain Lang. 2009;111(1):46-54. PMid:19356794. http://dx.doi.org/10.1016/j.bandl.2009.03.001.
http://dx.doi.org/10.1016/j.bandl.2009.0...
,1919 Kibby MY, Pavawalla SP, Fancher JB, Naillon AJ, Hynd GW. The relationship between cerebral hemisphere volume and receptive language functioning in dyslexia and Attention-Deficit/Hyperactivity Disorder. J Child Neurol. 2010;24(4):438-48. PMid:19211921. http://dx.doi.org/10.1177/0883073808324772.
http://dx.doi.org/10.1177/08830738083247...
,2727 Simos PG, Rezaie R, Fletcher JM, Juranek J, Passaro AD, Li Z, et al. Functional disruption of the brain mechanism for reading: effects of comorbidity and task difficulty among children with developmental learning problems. Neuropsychology. 2011;25(4):520-34. PMid:21574715. http://dx.doi.org/10.1037/a0022550.
http://dx.doi.org/10.1037/a0022550...
); one addressed neuropsychological performance in the inattentive and combined subtypes(2424 Londoño DMM, Cifuentes VV, Lubert CD. Caracterización neuropsicológica de una muestra de niños y niñas con tdah de la ciudad de Manizales. Biosalud. 2011;10(1):30-51.); one evaluated performance in executive and central coherence tasks(2222 Booth R, Happé F. “Hunting with a knife and . . . fork”: examining central coherence in autism, attention deficit/hyperactivity disorder, and typical development with a linguistic task. J Exp Child Psychol. 2010;107(4):377-93. PMid:20655060. http://dx.doi.org/10.1016/j.jecp.2010.06.003.
http://dx.doi.org/10.1016/j.jecp.2010.06...
); one focused on the perception of time, phonological skills, and executive function in ADHD(2626 Gooch D, Snowling M, Hulme C. Time perception, phonological skills and executive function in children with dyslexia and/or ADHD symptoms. J Child Psychol Psychiatry. 2011;52(2):195-203. PMid:20860755. http://dx.doi.org/10.1111/j.1469-7610.2010.02312.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
); and one investigated fine motor, sensory and perceptual functions(2323 Okuda PMM, Pinheiro FH, Germano GD, Padula NAMR, Lourencetti MD, Santos LCA, et al. Função motora fina, sensorial e perceptiva de escolares com transtorno do déficit de atenção com hiperatividade. J Soc Bras Fonoaudiol. 2011;23(4):351-7. PMid:22231056. http://dx.doi.org/10.1590/S2179-64912011000400010.
http://dx.doi.org/10.1590/S2179-64912011...
).

Regarding reading difficulties in ADHD, the importance of word recognition and decoding and reading speed for text comprehension was discussed in a study conducted in the United States(1515 Cutting LE, Materek A, Cole CAS, Levine TM, Mahone EM. Effects of fluency, oral language, and executive function on reading comprehension performance. Ann Dyslexia. 2009;59(1):34-54. PMid:19396550. http://dx.doi.org/10.1007/s11881-009-0022-0.
http://dx.doi.org/10.1007/s11881-009-002...
). According to the authors, slow reading might be associated with the increased demands of the processes involved in working memory, which would lead to difficulties in text processing and, consequently, in comprehension. In addition, failure in understanding would not be explained only by difficulty in word recognition and decoding, but by deficits related to oral language skills and executive function. Specifically, vocabulary, syntax, semantics, and phonological processing would be involved in the process of reading comprehension. As for the executive function, the authors point to the fact that deficits in the planning, working memory, organization, and inhibition skills may not be associated only with ADHD, but can be observed independently of the symptoms of this disorder. Therefore, the deficits related to the inference ability would be related not only to the semantic and syntactic aspects of oral language, but also to the processes of executive functioning.

In another study conducted in Brazil(1717 Silveira DC, Passos LMA, Santos PC, Chiappetta ALML. Avaliação da fluência verbal em crianças com transtorno da falta de atenção com hiperatividade: um estudo comparativo. Rev CEFAC. 2009;11(2):208-16.), the authors investigated the performance of children with and without ADHD through phonological verbal fluency and semantic verbal fluency tests. They verified that the performance of the ADHD group was similar to that of the control group, both in terms of phonological verbal fluency and semantic verbal fluency. Nevertheless, the ADHD group required additional time to initiate responses. In the same study, the authors investigated whether there would be a difference in performance between the ADHD subtypes - inattentive, hyperactive, and combined - and observed that the outcomes were not very relevant.

The correlation between Rapid Automatized Naming (RAN) and reading in children with and without ADHD was also analyzed(1818 Li JJ, Cutting LE, Ryan M, Zilioli M, Denckla MB, Mahone EM. Response variability in rapid automatized naming predicts reading comprehension. J Clin Exp Neuropsychol. 2009;31(7):877-88. PMid:19221923. http://dx.doi.org/10.1080/13803390802646973.
http://dx.doi.org/10.1080/13803390802646...
). The authors discuss, mainly, the existence of naming speed deficits in the disorder and suggest that the pause time in rapid naming tasks could predict reading fluency.

Processing speed and reading fluency, related to working memory in ADHD, were also discussed in another study(2525 Jacobson LA, Ryan M, Martin RB, Ewen J, Mostofsky SH, Denckla MB, et al. Working Memory Influences Processing Speed and Reading Fluency in ADHD. Child Neuropsychol. 2011;17(3):209-24. PMid:21287422. http://dx.doi.org/10.1080/09297049.2010.532204.
http://dx.doi.org/10.1080/09297049.2010....
). The researchers describe that children with ADHD who accurately decode words may still present poor reading fluency, compromising other cognitive processes. The outcomes of this study demonstrated that reading fluency and speed in children with ADHD were reduced in both silent reading and reading aloud.

The genetic risk related to ADHD and reading difficulties was discussed in international studies conducted with twins(2828 Greven CU, Rijsdijk FV, Asherson P, Plomin R. A longitudinal twin study on the association between ADHD symptoms and Reading. J Child Psychol Psychiatry. 2012;53(3):234-42. PMid:21819398. http://dx.doi.org/10.1111/j.1469-7610.2011.02445.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
,2929 Rosenberg J, Pennington BF, Willcutt EG, Olson RK. Gene by environment interactions influencing Reading Disability (RD) and the inattentive symptom dimension of Attention Deficit/Hyperactivity Disorder (ADHD). J Child Psychol Psychiatry. 2012;53(3):243-51. PMid:21884522. http://dx.doi.org/10.1111/j.1469-7610.2011.02452.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
). In one of these studies(2828 Greven CU, Rijsdijk FV, Asherson P, Plomin R. A longitudinal twin study on the association between ADHD symptoms and Reading. J Child Psychol Psychiatry. 2012;53(3):234-42. PMid:21819398. http://dx.doi.org/10.1111/j.1469-7610.2011.02445.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
), the authors referred to research that demonstrated the co-occurrence of both pathologies due to genetic risk factors. They also examined the longitudinal relationships between ADHD symptoms and reading difficulties, from childhood to adolescence, and verified an association between the symptoms and the difficulties attributable to shared genetic influences.

In another study conducted in the United States(2020 Willcutt EG, Betjemann RS, McGrath LM, Chhabildas NA, Olson RK, DeFries JC, et al. Etiology and neuropsychology of comorbidity between RD and ADHD: the case for multiple-deficit models. Cortex. 2010;46(10):1345-61. PMid:20828676. http://dx.doi.org/10.1016/j.cortex.2010.06.009.
http://dx.doi.org/10.1016/j.cortex.2010....
), the researchers discuss the unique deficit models for the explanation of complex pathologies such as ADHD and reading difficulties. In these models, the various risk factors - genetic, neuropsychological, and environmental - are disregarded for each disease and the comorbidities between the disorders cannot be explained. The authors indicate the existence of more than 20 proposed theoretical models to explain the occurrence of comorbidities between complex diseases, with ADHD and reading difficulties among them. ADHD is assessed through behavioral classifications, whereas reading difficulties are assessed by cognitive tests.

Furthermore, the symptoms that define these two pathologies do not overlap. The results confirmed the hypothesis that ADHD and reading disorder are related to multiple cognitive deficits and not to a single primary cognitive deficit. Reading difficulties would be associated with phonemic awareness, verbal reasoning, and working memory, whereas ADHD would be associated with inhibitory control. Both would share cognitive deficits related to processing speed because of genetic influences that would increase the risks of reading disability and ADHD.

Differences in the perception, detection, and discrimination of auditory and visual stimuli in children with ADHD were investigated in an international study(3030 Birkett EE, Talcott JB. Interval timing in children: effects of auditory and visual pacing stimuli and relationships with reading and attention variables. PLoS One. 2012;7(8):e42820. PMid:22900054. http://dx.doi.org/10.1371/journal.pone.0042820.
http://dx.doi.org/10.1371/journal.pone.0...
) that evaluated the production of motor responses in synchrony with external stimuli. According to this survey, the temporal processing related to the input of stimuli would be compromised in both ADHD and dyslexia. The authors emphasize that the tasks of motor synchronism allow the behavioral evaluation of the processing dimension, in which the precision and accuracy of the responses require cognitive abilities, and not the use of subjective judgments about the nature of the presented stimuli. Thus it would be possible to understand the cognitive mechanisms involved in developmental disorders, such as ADHD and dyslexia, which present deficits in temporal functions.

The results presented in the aforementioned study showed that the differences in performance in temporal processing tasks correlate with phenotypes of highly prevalent disorders, and that the use of visual tasks that require timing may be useful to demonstrate the quality of processing difficulties of children with ADHD and reading difficulties.

Regarding difficulties in mathematics and reading, two studies(1414 Raghubar K, Cirino P, Barnes M, Ewing-Cobbs L, Fletcher J, Fuchs L. Errors in multi-digit arithmetic and behavioral inattention in children with math difficulties. J Learn Disabil. 2009;42(4):356-71. PMid:19380494. http://dx.doi.org/10.1177/0022219409335211.
http://dx.doi.org/10.1177/00222194093352...
,2121 Hart SA, Petrill SA, Willcutt E, Thompson LA, Schatschneider C, Deater-Deckard K, et al. Exploring how symptoms of attention-deficit/hyperactivity are related to reading and mathematics performance: general genes, general environments. Psychol Sci. 2010;21(11):1708-15. PMid:20966487. http://dx.doi.org/10.1177/0956797610386617.
http://dx.doi.org/10.1177/09567976103866...
) addressed the coexistence of these difficulties in ADHD. In one of them(1414 Raghubar K, Cirino P, Barnes M, Ewing-Cobbs L, Fletcher J, Fuchs L. Errors in multi-digit arithmetic and behavioral inattention in children with math difficulties. J Learn Disabil. 2009;42(4):356-71. PMid:19380494. http://dx.doi.org/10.1177/0022219409335211.
http://dx.doi.org/10.1177/00222194093352...
), the researchers discuss performance in multi-digit arithmetic in children with difficulties in mathematics. The performance mentioned by the authors includes comprehension of the types of errors committed and the understanding that these errors may vary as a function of reading, severity of problems in mathematics, or presence of attention problems. The performance of children with typical development in arithmetic suggests that the errors made by them can provide clues about the procedural and conceptual knowledge used, aspects that would be impaired in ADHD.

With respect to the relationship between brain structures and language changes in ADHD(1616 Kibby MY, Kroese JM, Krebbs H, Hill CE, Hynd GW. The pars triangularis in dyslexia and ADHD: a comprehensive approach. Brain Lang. 2009;111(1):46-54. PMid:19356794. http://dx.doi.org/10.1016/j.bandl.2009.03.001.
http://dx.doi.org/10.1016/j.bandl.2009.0...
,1919 Kibby MY, Pavawalla SP, Fancher JB, Naillon AJ, Hynd GW. The relationship between cerebral hemisphere volume and receptive language functioning in dyslexia and Attention-Deficit/Hyperactivity Disorder. J Child Neurol. 2010;24(4):438-48. PMid:19211921. http://dx.doi.org/10.1177/0883073808324772.
http://dx.doi.org/10.1177/08830738083247...
,2727 Simos PG, Rezaie R, Fletcher JM, Juranek J, Passaro AD, Li Z, et al. Functional disruption of the brain mechanism for reading: effects of comorbidity and task difficulty among children with developmental learning problems. Neuropsychology. 2011;25(4):520-34. PMid:21574715. http://dx.doi.org/10.1037/a0022550.
http://dx.doi.org/10.1037/a0022550...
), one of the studies showed that there is no reduction of brain volume in children with ADHD and dyslexia, as well as in children with only ADHD, or with only dyslexia(1919 Kibby MY, Pavawalla SP, Fancher JB, Naillon AJ, Hynd GW. The relationship between cerebral hemisphere volume and receptive language functioning in dyslexia and Attention-Deficit/Hyperactivity Disorder. J Child Neurol. 2010;24(4):438-48. PMid:19211921. http://dx.doi.org/10.1177/0883073808324772.
http://dx.doi.org/10.1177/08830738083247...
). However, in the group of children with difficulties in receptive language, associated with dyslexia and ADHD, asymmetry between the right and left hemispheres was found in the comparison with children without comprehension deficits. Another study(1616 Kibby MY, Kroese JM, Krebbs H, Hill CE, Hynd GW. The pars triangularis in dyslexia and ADHD: a comprehensive approach. Brain Lang. 2009;111(1):46-54. PMid:19356794. http://dx.doi.org/10.1016/j.bandl.2009.03.001.
http://dx.doi.org/10.1016/j.bandl.2009.0...
), which discussed the possibility of participation of the region called pars triangularis in phonological processing, showed that children with dyslexia did not present changes in the shape and length of this structure. In contrast, children with ADHD presented alterations in the length of the studied region. According to the authors, the size of the pars triangularis structure would be predictive of good performance in phonological awareness skills and in RAN tasks.

Another international study(2727 Simos PG, Rezaie R, Fletcher JM, Juranek J, Passaro AD, Li Z, et al. Functional disruption of the brain mechanism for reading: effects of comorbidity and task difficulty among children with developmental learning problems. Neuropsychology. 2011;25(4):520-34. PMid:21574715. http://dx.doi.org/10.1037/a0022550.
http://dx.doi.org/10.1037/a0022550...
) reported that children with reading disability presented decreased amplitude of neurophysiological activity in the upper temporal gyrus, bilaterally, and in the left supramarginal region of the angular gyrus. These findings were mainly revealed by the pseudoword reading tasks. The authors note that no changes were observed in the group of children with only ADHD.

With regard to the neuropsychological performance of children with ADHD, another study(2424 Londoño DMM, Cifuentes VV, Lubert CD. Caracterización neuropsicológica de una muestra de niños y niñas con tdah de la ciudad de Manizales. Biosalud. 2011;10(1):30-51.), conducted in Colombia, investigated the neuropsychological performance characteristics of children with ADHD, inattentive and combined subtypes, and without ADHD. The main results showed differences in the performance of children with ADHD, compared with those of the control group, in metalinguistic abilities and in tasks that evaluated selective attention. The mean of the results presented by the group of children with ADHD, combined subtype, was lower than that presented by the group of children with ADHD, inattentive subtype, in these tasks. As for the results in tasks of executive functions and memory, as well as in the intellectual capacity assessment, no significant differences were found between the ADHD group and the control group.

The performance of children with ADHD in the task of completing sentences and in executive task was evaluated in an international study(2222 Booth R, Happé F. “Hunting with a knife and . . . fork”: examining central coherence in autism, attention deficit/hyperactivity disorder, and typical development with a linguistic task. J Exp Child Psychol. 2010;107(4):377-93. PMid:20655060. http://dx.doi.org/10.1016/j.jecp.2010.06.003.
http://dx.doi.org/10.1016/j.jecp.2010.06...
). The task of completing sentences verifies whether there will be consistency in the words chosen by the child to complete the proposed sentences. The results of the study showed that the group with ADHD presented good performance in this task compared with the control group, composed of children diagnosed with ASD, and with the group of children with typical development. Regarding the executive task, the group with ADHD presented worse performance than the other groups, evidencing that the problems related to inhibition would not be related to the performance in tasks of central coherence.

Another international study(2626 Gooch D, Snowling M, Hulme C. Time perception, phonological skills and executive function in children with dyslexia and/or ADHD symptoms. J Child Psychol Psychiatry. 2011;52(2):195-203. PMid:20860755. http://dx.doi.org/10.1111/j.1469-7610.2010.02312.x.
http://dx.doi.org/10.1111/j.1469-7610.20...
) investigated the perception of time, phonological abilities, and the executive function in four groups of children: those with only dyslexia, those with only ADHD symptoms, those with dyslexia and ADHD symptoms, and those who were part of the control group, with typical development. The results found in the study suggest that dyslexia and ADHD symptoms are associated with distinct cognitive profiles. In this sense, children with dyslexia or symptoms of ADHD, such as comorbidities, present an additive combination of cognitive deficits, associated only with dyslexia or only with the symptoms of ADHD. The deficits in duration discrimination associated with dyslexia are mediated by symptoms of inattention resulting from the comorbidity between these disorders. The authors emphasize the importance of considering the impact of ADHD symptoms when investigating the neuropsychological profile of children with dyslexia.

The fine motor, sensory and perceptual functions of schoolchildren with ADHD and of students with good school performance and without behavioral changes were evaluated in a survey conducted in Brazil(2323 Okuda PMM, Pinheiro FH, Germano GD, Padula NAMR, Lourencetti MD, Santos LCA, et al. Função motora fina, sensorial e perceptiva de escolares com transtorno do déficit de atenção com hiperatividade. J Soc Bras Fonoaudiol. 2011;23(4):351-7. PMid:22231056. http://dx.doi.org/10.1590/S2179-64912011000400010.
http://dx.doi.org/10.1590/S2179-64912011...
). The results of this study showed that students with ADHD presented dysgraphia and delay in the development of fine motor, sensory and perceptual coordination. The authors attribute these changes to neurological dysfunctions in the frontal-striatal-cerebellar region, which is also related to the planning, organization, and execution of the motor act. Fine motor, sensory and perceptual alterations would hinder bimanual coordination, manual dexterity, dissociation, and motor precision, which would justify the occurrence of dysgraphia in children with ADHD and would compromise the process of acquisition and learning of writing.

Analysis of the observational studies

Regarding the analysis of the observational studies, according to the STROBE Statement, it was possible to verify that most of the studies were partly compliant with the proposed criteria, mainly with respect to the sections Methodology and Results.

This result may be suggestive of difficulties related to the existence of a consensus about the Speech-language Pathology disorders found in ADHD, as well as about the instruments necessary for the evaluation of these alterations. The fact that some studies do not comply with the criteria for Methodology may generate impairment in the reproducibility of Method in other studies. Concerning the criteria not met regarding Results, there may be impairment in the general understanding of the study.

CONCLUSION

The study of the scientific productions revealed that the Speech-language Pathology disorders most frequently addressed in Attention Deficit Hyperactivity Disorder (ADHD) were reading disorders, followed by changes in auditory processing. However, it was not possible to establish a profile of changes in patients with ADHD. There is a need for the participation of speech-language pathologists in the teams that evaluate children and adolescents with symptoms of ADHD considering that Speech-language Pathology disorders are present in most cases.

  • Study carried out at Programa de Pós-graduação em Ciências Fonoaudiológicas, Faculdade de Medicina, Universidade Federal de Minas Gerais – UFMG - Belo Horizonte (MG), Brazil.
  • Financial support: Fundação de Amparo à Pesquisa do Estado de Minas Gerais – FAPEMIG.

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Publication Dates

  • Publication in this collection
    Dec 2016

History

  • Received
    02 Nov 2015
  • Accepted
    10 Dec 2015
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