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The broad autism phenotype in parents of individuals with autism: a systematic review of the literature

O fenótipo ampliado do autismo em pais de indivíduos autistas: uma revisão sistemática da literatura

Abstracts

The broad autism phenotype (BAP) is a milder manifestation of the defining symptoms of the syndrome in individuals without autism. This study conducted a systematic review of studies about behavioral characteristics of interpersonal relationships, communication and rigidity, as well as about three cognitive models, Theory of Mind, central coherence and executive function, in parents of individuals with autism. The indexed databases were LILACS, IBECS, Web of Science, and MEDLINE, and the studies retrieved were published between 1991 and March 2012. Parents of individuals with autism have more difficulties in interpersonal relationships and in pragmatic language use and have more rigidity traits. The inclusions of the cognitive theories in the group of BAP characteristics were inconclusive.

Autism-spectrum disorder; phenotype; endophenotypes; parents


O fenótipo ampliado do autismo (FAA) é a manifestação atenuada de características qualitativamente similares às que definem a síndrome, em indivíduos não portadores do transtorno. O objetivo deste artigo é realizar uma revisão sistemática de estudos que abordam as características comportamentais relacionadas a interação social, comunicação e rigidez, além dos modelos cognitivos Teoria da Mente (Theory of Mind, ToM), coerência central e funções executivas, em pais de indivíduos autistas. As bases de dados consultadas foram: LILACS, IBECS, Web of Science e MEDLINE; foram selecionados estudos publicados entre 1991 e março de 2012. Os resultados apontaram que os pais de indivíduos autistas possuem déficits na interação social, na linguagem pragmática e traços de rigidez. A inclusão dos modelos cognitivos do autismo no grupo de características que compõem o FAA permanece inconclusiva.

Transtorno autístico; fenótipo; endofenótipos; pais


Introduction

Childhood autism is a behavioral syndrome characterized by a triad of symptoms: deficits in social interactions, deficits in verbal and non-verbal communication and inflexible, restricted and stereotyped behaviors and interests.11. American Psychiatric Association. Manual de diagnóstico e estatística das doenças mentais - 4ª edição. Porto Alegre: Artmed; 2002. The intensity of these symptoms may vary from mild, in which individual have a high intellectual potential, to severe, in which there is mental retardation and lack of speech.22. Wing L. The continuum of autistic characteristics. In: Schopler E, Mesibov GB, editors. Diagnosis and assessment in autism. New York: Plenum Press; 1988.

For many years autism was believed to be a psychological disorder explained by relationship models. However, as genetic studies advanced, the understanding that children have autism due to their parents' affective distance is no longer accepted.33. Klin A. Autismo e síndrome de Asperger: uma visão geral. Rev Rev Psiquiatr Rio Gd Sul. 2006;28:47-53. We currently know that it is a complex, highly hereditary neurobiological syndrome.

Studies have indicated that relatives of people with autism also have autism traits at a lesser degree than that found in high-functioning autism, but at an intensity that is very mild and does not characterize the disorder.44. Sucksmith E, Roth I, Hoekstra RA. Autistic traits below the clinical threshold: re-examining the broader autism phenotype in the 21st century. Neuropsychol Rev. 2011;21:360-89. , 55. Gerdts J, Bernier R. The broader autism phenotype and its implications on the etiology and treatment of autism spectrum disorders. Autism Res Treat. 2011;2011:545901. These mild expressions in individuals without the syndrome have been named the broad autism phenotype (BAP).66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. The prevalence of the BAP in families ranges from 12 to 30%,66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.

7. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.

8. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90.
- 99. Pickles A, Starr E, Kazak S, Bolton P, Papanikolaou K, Bailey A, et al. Variable expression of the autism broader phenotype: findings from extended pedigrees J Child Psychol Psychiatry. 2000;41:491-502. and male parents have more BAP characteristics than mothers.77. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6. , 1010. Scheeren AM, Stauder JE. Broader autism phenotype in parents of autistic children: reality or myth? J Autism Dev Disord. 2008;38:276-87. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9.

The importance of studying phenotypes and endophenotypes of psychiatric syndromes has been highlighted in the literature. These characteristics may be useful in the identification of the genes that confer vulnerability to these disorders.1212. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636-45. Additionally, studies about the BAP of parents may contribute to the definition of diagnostic criteria, may refine the understanding of some symptoms when subdomains are detected in each factor, and may contribute to the definition of treatments. Moreover, parents may also benefit from some interventions.

Although the term is BAP, this concept also includes the possible endophenotype of the syndrome. Phenotypes are the observable characteristics or behaviors that result from gene expression, environmental influences and the interaction between both,1212. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636-45. and which correspond to the triad of core symptoms in the case of autism. Endophenotypes, in contrast, are manifestations of the genotype without the influence of the environment. They are subclinical inherited markers of the disease that may be neurophysiological, biochemical, endocrinological, neuroanatomic or cognitive. They involve fewer genes than those in the disorder itself, and are expressed in the person that has the gene even when the syndrome is not manifest. They are hereditary and more often found in the parents of patients with the disorder than in the general population.1313. Viding E, Blakemore SJ. Endophenotype approach to developmental psychopathology: implications for autism research. Behav Genet. 2007;37:51-60.

In autism, there is a cognitive abnormality (endophenotype) associated with behaviors for each behavioral symptom (phenotype). The models of cognitive deficits, possibly responsible for dysfunctional behaviors, are: Theory of Mind (ToM) deficit, weak central coherence and impaired executive functions.1414. Happé F, Frith U. The neuropsychology of autism. Brain. 1996;119:1377-1400. These three theories are complementary, and each explains some core features of the disorder better than others.1515. Happé F, Ronald A, Plomin R. Time to give up on a single explanation for autism. Nat Neurosci. 2006;9:1218-20.

This study reviewed studies that investigated the behavioral characteristics of the triad of core symptoms, as well as the three main cognitive theories (ToM, central coherence and executive functions deficits) in the parents of children with autism to identify which features belong to the BAP in this group of individuals.

Method

This review was conducted in the second half of 2012 using the following electronic databases: LILACS and IBECs - databases of Latin American and Caribbean health sciences literature; Web of Science and MEDLINE - databases of international literature. Studies published between 1991 and March 2012 were analyzed. The keywords used were all related to phenotype, endophenotype, autism, parents and family. The total number of studies retrieved in the search, as well as the keywords used in each database, is shown in table 1.

Table 1
Keywords used in electronic databases to retri eve studies published between 1991 and March 2012

Studies were selected according to the following inclusion criteria: a) published in Portuguese, English or Spanish; b) object of study was the cognitive and behavioral characteristics of autism in parents of individuals with autism; c) original studies. Exclusion criteria were: a) studies about genetics that did not investigate autism phenotype or endophenotype; b) studies that included only siblings; c) studies that evaluated the BAP in the general population; d) studies that investigated endophenotype according to biological or neurofunctional dimensions; e) studies that evaluated only parents of individuals with pervasive developmental disorders other than autism; f) studies that evaluated the BAP using only personality traits of parents; g) studies that evaluated the BAP only according to presence of other psychiatric disorders in parents; h) opinion papers; i) studies that used non-standardized instruments; j) studies that did not include a control group.

According to the inclusion and exclusion criteria, the abstracts of all eligible studies were read by two independent examiners (LC and WC). Divergent opinions were discussed by the two until a consensus was reached. After the studies had been selected, their complete texts were read. Data about all studies were organized in tables for the analysis of objectives and hypothesis, methods, including the description of the sample and the instruments used, and, finally, results and conclusions. Therefore, the main ideas expressed in each study, as well as convergent and divergent findings, were analyzed qualitatively and descriptively, and data were interpreted and analyzed. Secondary references found in the studies retrieved from the databases were also used.

Results

A total of 417 studies were retrieved: 368 were not included due to exclusion criteria or were not about the topic under study. Most of the studies excluded were about genetics (164 studies), syndromes that had some association with autism, such as the Rett syndrome (71 studies), or phenotype expression in individuals with autism (54 studies). The other 79 studies met other exclusion criteria, and 19 were repeated studies.

After reading the 27 studies originally selected, 8 other studies were found in their references. A total of 35 studies were included. Some also evaluated other family members, but their results were only about behavioral characteristics and cognitive models of parents of individuals with autism. Information about other relatives, as well as information about other constructs, was not included in the tables or text below. Two studies1010. Scheeren AM, Stauder JE. Broader autism phenotype in parents of autistic children: reality or myth? J Autism Dev Disord. 2008;38:276-87. , 1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. are repeated in the two tables because they evaluated both behavioral and cognitive characteristics. Therefore, although only 35 studies were selected, the two tables show a total of 37 studies: 19 about behavioral characteristics and 18 about cognitive models.

Behavioral characteristics in the triad of core symptoms

We reviewed what instruments were used to evaluate behavioral characteristics. Those that evaluated the BAP globally, that is, that included the three core domains of the syndrome, are shown in Table 2. In the 35 studies reviewed, only four instruments were used to evaluate the triad of core symptoms in parents: the Family History Interview (FHI),1717. Bolton P, Macdonald H, Pickles A, Rios P, Goode S, Crowson M, et al. A case-control family history study of autism. J Child Psychol Psychiatry. 1994;35:877-900. the Autism Spectrum Quotient (AQ),1818. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord. 2001;31:5-17. the Broader Phenotype Autism Symptom Scale (BPASS),1919. Dawson G, Estes A, Munson J, Schellenberg G, Bernier R, Abbott R. Quantitative assessment of autism symptom-related traits in probands and parents: Broader Phenotype Autism Symptom Scale. J Autism Dev Disord. 2007;37:523-36. and the Broad Autism Phenotype Questionnaire (BAPQ).88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. FHI was the first instrument used for this purpose and was the most frequently used in studies up to 2000. Today, the questionnaire most often used in the AQ. Other instruments also evaluate isolated behavioral characteristics, and of the three domains, language is the one evaluated in most instruments.

Table 2
Description of the i nstruments used to ev aluate the BAP gl obally among parents of i ndividuals with autism

The selected studies about behavioral characteristics of parents of individuals with autism are listed in Table 3.

Table 3
Studies about the beha vioral characteristics of parents of i ndividuals with autism

Changes in social interaction

Seven articles evaluated social relationships of parents of individuals with autism.77. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6. , 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9. , 2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90. , 2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. , 2626. Baron-Cohen S, Bolton P, Wheelwright S, Scahill V, Short L, Mead G, et al. Autism occurs more often in families of physicists, engineers, and mathematicians. Autism. 1998;2:296-301. , 2828. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33. None of these studies evaluated only this domain, and social interaction was evaluated together with other behavioral characteristics. Moreover, social difficulties were approached according to different dimensions, and each study had a specific observation focus of the social functioning of parents of individuals with autism.

Some studies evaluated the interest of parents in social interactions,88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. and others evaluated social skills.77. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6. Results demonstrated that some individuals prefer not to interact and are aloof,88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. whereas others do want to interact, but are not able to do it satisfactorily.

Losh et al.2828. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33. found that 23% of the parents of multiple-incidence autism families do not have friends, in contrast with 11% of parents of single-incidence autism families and 3% of parents of children with Down syndrome. High rates of social difficulty in multiple-incidence autism families were also found in the studies conducted by Bernier et al.2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. and Piven et al.66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. , 2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90. Moreover, parents of children with autism had limited friendships66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. and often worked in fields that require little social understanding, such as math, engineering and physics.2626. Baron-Cohen S, Bolton P, Wheelwright S, Scahill V, Short L, Mead G, et al. Autism occurs more often in families of physicists, engineers, and mathematicians. Autism. 1998;2:296-301.

Language and communication impairments

Sixteen studies evaluated the communicative characteristics of parents of individuals with autism.66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.

7. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.
- 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9. , 1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. , 2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90.

21. Fombonne E, Bolton P, Prior J, Jordan H, Rutter M. A family study of autism: cognitive patterns and levels in parents and siblings. J Child Psychol Psychiatry. 1997;38:667-83.

22. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28.

23. Whitehouse AJ, Barry JG, Bishop DV. The broader language phenotype of autism: a comparison with specific language impairment. J Child Psychol Psychiatry. 2007;48:822-30.

24. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20.
- 2525. Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychol Med. 1992;22:245-54. , 2727. Ruser TF, Arin D, Dowd M, Putnam S, Winklosky B, Rosen-Sheidley B, et al. Communicative competence in parents of children with autism and parents of children with specific language impairment. J Autism Dev Disord. 2007;37:1323-36. , 2929. Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC. Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008;30:557-67.

30. Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38.

31. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74.
- 3232. Bishop DV, Maybery M, Wong D, Maley A, Hill W, Hallmayer J. Are phonological processing deficits part of the broad autism phenotype? Am J Med Genet B Neuropsychiatr Genet. 2004;128B:54-60. Seven studies evaluated this domain together with others (social domain and rigidity),66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.

7. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.
- 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9. , 2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90. , 2222. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28. , 2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. and nine were specially designed to evaluate communicative skills.1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. , 2121. Fombonne E, Bolton P, Prior J, Jordan H, Rutter M. A family study of autism: cognitive patterns and levels in parents and siblings. J Child Psychol Psychiatry. 1997;38:667-83. , 2323. Whitehouse AJ, Barry JG, Bishop DV. The broader language phenotype of autism: a comparison with specific language impairment. J Child Psychol Psychiatry. 2007;48:822-30. , 2525. Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychol Med. 1992;22:245-54. , 2727. Ruser TF, Arin D, Dowd M, Putnam S, Winklosky B, Rosen-Sheidley B, et al. Communicative competence in parents of children with autism and parents of children with specific language impairment. J Autism Dev Disord. 2007;37:1323-36. , 2929. Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC. Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008;30:557-67.

30. Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38.

31. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74.
- 3232. Bishop DV, Maybery M, Wong D, Maley A, Hill W, Hallmayer J. Are phonological processing deficits part of the broad autism phenotype? Am J Med Genet B Neuropsychiatr Genet. 2004;128B:54-60. Seven evaluated structural language abnormalities2121. Fombonne E, Bolton P, Prior J, Jordan H, Rutter M. A family study of autism: cognitive patterns and levels in parents and siblings. J Child Psychol Psychiatry. 1997;38:667-83. , 2222. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28. , 2727. Ruser TF, Arin D, Dowd M, Putnam S, Winklosky B, Rosen-Sheidley B, et al. Communicative competence in parents of children with autism and parents of children with specific language impairment. J Autism Dev Disord. 2007;37:1323-36. , 2929. Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC. Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008;30:557-67.

30. Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38.

31. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74.
- 3232. Bishop DV, Maybery M, Wong D, Maley A, Hill W, Hallmayer J. Are phonological processing deficits part of the broad autism phenotype? Am J Med Genet B Neuropsychiatr Genet. 2004;128B:54-60. and nine, the social use of language (pragmatic language)66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.

7. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.
- 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9. , 1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. , 2222. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28. , 2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. , 2525. Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychol Med. 1992;22:245-54. , 3131. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74.; some evaluated these two communicative characteristics. Although structural language abnormalities are not classified as behavioral characteristics, they were included in this section because they lead to communicative deficits.

In a pioneering study, Landa et al.2525. Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychol Med. 1992;22:245-54. evaluated communication of parents and found three groups of pragmatic abnormalities measured by means of the Pragmatic Rating Scale (PRS): disinhibited social communication, awkward/inadequate expressions and odd verbal interactions. Since that study, pragmatic language skills have been broadly investigated, which corroborates the idea that parents of children with autism have social communication difficulties.66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.

7. Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.
- 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 1111. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9. , 1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. , 2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. , 2727. Ruser TF, Arin D, Dowd M, Putnam S, Winklosky B, Rosen-Sheidley B, et al. Communicative competence in parents of children with autism and parents of children with specific language impairment. J Autism Dev Disord. 2007;37:1323-36.

Abnormalities associated with structural language have also been evaluated in groups of parents. Whitehouse et al.2323. Whitehouse AJ, Barry JG, Bishop DV. The broader language phenotype of autism: a comparison with specific language impairment. J Child Psychol Psychiatry. 2007;48:822-30. evaluated language deficits and found that parents of children with autism and parents of typically-developing children had similar performances, and that both groups had a better performance than that of parents of children with specific language impairments (SLI). Therefore, the difficulties associated with structural language are not found in the BAP of parents. This finding has been confirmed by the studies conducted by Bishop et al.,3232. Bishop DV, Maybery M, Wong D, Maley A, Hill W, Hallmayer J. Are phonological processing deficits part of the broad autism phenotype? Am J Med Genet B Neuropsychiatr Genet. 2004;128B:54-60. Whitehouse et al.,3131. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74. and Lindgren et al.3030. Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38. However, other studies have found phonological processing deficits among parents of individuals with autism, which supports the hypothesis that these deficits are part of the BAP.2929. Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC. Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008;30:557-67.

The analysis of reading and writing acquisition revealed that the difficulties of some parents of children with autism seem to be associated with an abnormal development of language rather than with autism.2121. Fombonne E, Bolton P, Prior J, Jordan H, Rutter M. A family study of autism: cognitive patterns and levels in parents and siblings. J Child Psychol Psychiatry. 1997;38:667-83. In the study conducted by Folstein et al. in 1999,2222. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28. only the parents with a history of cognitive deficits associated with language in childhood had a poorer performance in reading and writing tasks than parents of individuals with Down syndrome. A history of language delays and deficits in childhood in the group of individuals with autism was also reported by Piven et al.2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90.

Pragmatic language deficits may be seen as a reliable characteristic of the BAP. However, other language deficits, such as delays and difficulties in reading and writing acquisition and difficulties in structural language use, although present in some of the parents of children with autism, have not been confirmed to be part of the BAP,2323. Whitehouse AJ, Barry JG, Bishop DV. The broader language phenotype of autism: a comparison with specific language impairment. J Child Psychol Psychiatry. 2007;48:822-30. , 3030. Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38. , 3131. Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74. and further studies should be conducted to investigate this topic.

Restricted interests and repetitive and stereotyped behavior

Of the three core symptoms of autism, this is the one with the smallest number of studies that evaluated parents. Only five studies were retrieved.66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. , 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. , 2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90. , 2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. , 2828. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33. Moreover, this domain has only one category, divided into different characteristics: intense restricted interests; adherence to routines and rituals; stereotyped and repetitive motor mannerisms; and persistent preoccupation with parts of objects.11. American Psychiatric Association. Manual de diagnóstico e estatística das doenças mentais - 4ª edição. Porto Alegre: Artmed; 2002. Although it is a single category, the behaviors described here are substantially heterogeneous, but the main studies using questionnaires to detect BAP characteristics in parents have not defined this subdomain classification.

In the studies conducted by Piven et al.,66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. Hurley et al.,88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. and Losh et al.,2828. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33. rigidity describes resistance to changes and a strong attachment to routines. Bernier et al.2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. evaluated behavioral flexibility and range of interests. Piven et al.,2020. Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90. in turn, evaluated restricted interests and rigidity, or perfectionism. No study included stereotyped and repetitive motor mannerisms in the evaluation of parents. Questionnaires evaluated the same domain in different ways.

The hypothesis that parents also have a rigid personality, with little interest in what is new, as well as with difficulties in dealing with routine changes, has been confirmed in some studies.66. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411. , 88. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90. In the study conducted by Bernier et al.2424. Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20. only parents of multiple-incidence autism families had characteristics of rigidity. Losh et al.,2828. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33. however, found that parents of multiple-incidence autism families had more characteristics of rigidity than parents that had only one child with autism, who, in turn, had more autism traits than parents in the control group.

Cognitive models

Eighteen studies evaluated central coherence, executive functions and ToM in groups of parents of individuals with autism, and most included more than one cognitive model. Table 4 describes these studies.

Table 4
Studies about cogni tive models: executive functions, central coherence and ToM among parents of chi ldren with autism

Central coherence

The theory that individuals with autism have a weak central coherence, developed by Frith in 1989,4949. Frith U. Autism: Explaining the enigma. Oxford: Blackwell; 1989. suggests that most people that do not have autism-spectrum disorder have a natural and spontaneous tendency to integrate details into a global entity and to process information received according to its context, observing and recalling more of the general picture than of the details. In contrast, people with autism-spectrum disorder seem to have a deficit in local processing and often miss the general meaning. However, different from other cognitive theories, the theory of a weak central coherence does not define deficits; rather, it claims that strong and weak central coherence have advantages and disadvantages and are merely different cognitive styles.5050. Happé F. Autism: cognitive deficit or cognitive style? Trends Cogn Sci. 1999;3: 216-22. Initially, this theory attempted to explain all the core symptoms of autism. However, after several studies that supported, or not, this hypothesis, it is currently seen as one of the cognitive styles found in the disorder, which contributes, therefore, to the view that autism includes multiple deficits.1515. Happé F, Ronald A, Plomin R. Time to give up on a single explanation for autism. Nat Neurosci. 2006;9:1218-20.

In addition to visual and spatial skills, the central coherence cognitive models also include verbal skills. Individuals with a weak central coherence have more difficulties in understanding words by means of their context, which, therefore, contributes to a deficit in communication.5151. 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;107:377-93. Some studies found abnormalities in central coherence tests only when evaluating verbal skills and not, therefore, in tests of visual skills.4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.

The theory of a weak central coherence, although logical and convincing, remains inconsistent in the case of parents of individuals with autism. Six studies evaluated this cognitive model,1010. Scheeren AM, Stauder JE. Broader autism phenotype in parents of autistic children: reality or myth? J Autism Dev Disord. 2008;38:276-87. , 3636. Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307. , 3838. Bölte S, Poustka F. The broader cognitive phenotype of autism in parents: how specific is the tendency for local processing and executive dysfunction? J Child Psychol Psychiatry. 2006;47:639-45. , 3939. de Jonge MV, Kemner C, van Engeland H. Superior disembedding performance of high-functioning individuals with autism spectrum disorders and their parents: the need for subtle measures. J Autism Dev Disord. 2006;36:677-83. , 4545. de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205. , 4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26. but only two evaluated verbal characteristics.3636. Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307. , 4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26. Results have been inconclusive, as authors constantly apply the same instruments to different samples and find different results.3636. Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307. , 4545. de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205. Bölte & Poustka3838. Bölte S, Poustka F. The broader cognitive phenotype of autism in parents: how specific is the tendency for local processing and executive dysfunction? J Child Psychol Psychiatry. 2006;47:639-45. evaluated central coherence skills of parents of children with autism and found a better performance in the Embedded Figures test, but not in the block design test. They found that the improved skill of people with autism to identify simple forms embedded in complex figures seems to be the main characteristic of local processing. Therefore, they suggest that this skill may be a characteristic of the BAP. Jonge et al.3939. de Jonge MV, Kemner C, van Engeland H. Superior disembedding performance of high-functioning individuals with autism spectrum disorders and their parents: the need for subtle measures. J Autism Dev Disord. 2006;36:677-83. found that fathers performed better than control parents only in number of attempts to find the correct answer in the Embedded Figures test. However, the same authors conducted a study to evaluate central coherence of parents using the block design test and did not find differences between groups.4545. de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205.

Happé et al.3636. Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307. evaluated parents of children with autism using a battery of tasks and found that fathers had a weak central coherence according to visual and verbal tasks. However, in the same study, mothers had abnormal results only in verbal tasks. Their findings of unequal results for different sexes are inconclusive, according to the authors, because of the small sample size.

Other studies did not find any differences between parents of individuals with autism and other groups of parents, and their authors suggest that parents of individuals with autism have deficits in local processing, or a weak central coherence.1010. Scheeren AM, Stauder JE. Broader autism phenotype in parents of autistic children: reality or myth? J Autism Dev Disord. 2008;38:276-87. , 4545. de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205. However, their studies included only tests that evaluated visual skills. Losh et al.4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26. also did not find any differences in visual skills between groups of parents, but difference were detected in verbal skills.

Executive functions

Executive functions are a set of integrated skills that allow individuals to direct their behavior to goals, to monitor efficiency and adequacy of these behaviors, to drop inefficient strategies and, therefore, to solve immediate, medium-term and long-term problems.5252. Malloy-Diniz LF, Sedo M, Fuentes D, Leite WB. Neuropsicologia das funções executivas. In: Fuentes D, Malloy-Diniz L, Camargos CP, Cosenza RM, editors. Neuropsicologia: teoria e prática. Porto Alegre: Artmed; 2008. Individuals with autism have deficits in these cognitive skills, which may be responsible for a high level of rigidity and perseveration,5353. Hill EL. Executive dysfunction in autism. Trends Cogn Sci. 2004;8:26-32. as well as for the performance of rituals and difficulties in dealing with changes in their routines. According to the seven studies retrieved,3333. Szatmari P, Georgiades S, Duku E, Zwaigenbaum L, Goldberg J, Bennett T. Alexithymia in parents of children with autism spectrum disorder. J Autism Dev Disord. 2008;38:1859-65.

34. Piven J, Palmer P. Cognitive deficits in parents from multiple-incidence autism families. J Child Psychol Psychiatry. 1997;38:1011-21.
- 3535. Hughes C, Leboyer M, Bouvard M. Executive function in parents of children with autism. Psychol Med. 1997;27:209-20. , 4141. Wong D, Maybery M, Bishop DV, Maley A, Hallmayer J. Profiles of executive function in parents and siblings of individuals with autism spectrum disorders. Genes Brain Behav. 2006;5:561-76. , 4242. Delorme R, Goussé V, Roy I, Trandafir A, Mathieu F, Mouren-Siméoni MC, et al. Shared executive dysfunctions in unaffected relatives of patients with autism and obsessive-compulsive disorder. Eur Psychiatry. 2007;22:32-8. , 4444. Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53. , 4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26. parents of individuals with autism also have deficits in executive functions, particularly those associated with planning3434. Piven J, Palmer P. Cognitive deficits in parents from multiple-incidence autism families. J Child Psychol Psychiatry. 1997;38:1011-21. , 3535. Hughes C, Leboyer M, Bouvard M. Executive function in parents of children with autism. Psychol Med. 1997;27:209-20. , 4242. Delorme R, Goussé V, Roy I, Trandafir A, Mathieu F, Mouren-Siméoni MC, et al. Shared executive dysfunctions in unaffected relatives of patients with autism and obsessive-compulsive disorder. Eur Psychiatry. 2007;22:32-8. (however, see Wong et al.4141. Wong D, Maybery M, Bishop DV, Maley A, Hallmayer J. Profiles of executive function in parents and siblings of individuals with autism spectrum disorders. Genes Brain Behav. 2006;5:561-76. and Losh et al.4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.); difficulties in operational memory4444. Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53. (however, see Wong et al.4141. Wong D, Maybery M, Bishop DV, Maley A, Hallmayer J. Profiles of executive function in parents and siblings of individuals with autism spectrum disorders. Genes Brain Behav. 2006;5:561-76.); cognitive flexibility3535. Hughes C, Leboyer M, Bouvard M. Executive function in parents of children with autism. Psychol Med. 1997;27:209-20. (however, see Bishop et al.,3333. Szatmari P, Georgiades S, Duku E, Zwaigenbaum L, Goldberg J, Bennett T. Alexithymia in parents of children with autism spectrum disorder. J Autism Dev Disord. 2008;38:1859-65. Delorme et al.,4242. Delorme R, Goussé V, Roy I, Trandafir A, Mathieu F, Mouren-Siméoni MC, et al. Shared executive dysfunctions in unaffected relatives of patients with autism and obsessive-compulsive disorder. Eur Psychiatry. 2007;22:32-8. Losh et al.4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.); and verbal and non-verbal fluency4141. Wong D, Maybery M, Bishop DV, Maley A, Hallmayer J. Profiles of executive function in parents and siblings of individuals with autism spectrum disorders. Genes Brain Behav. 2006;5:561-76. (however, see Delorme et al.4242. Delorme R, Goussé V, Roy I, Trandafir A, Mathieu F, Mouren-Siméoni MC, et al. Shared executive dysfunctions in unaffected relatives of patients with autism and obsessive-compulsive disorder. Eur Psychiatry. 2007;22:32-8.).

Although several studies confirm the presence of deficits in executive functions of parents of individuals with autism and their children, these deficits are not associated only with this disorder,5353. Hill EL. Executive dysfunction in autism. Trends Cogn Sci. 2004;8:26-32. which raises questions about what role they may have in explaining the behavioral abnormalities found in autism.

Theory of Mind

Theory of Mind (ToM) is the main cognitive model of the social impairments of individuals with autism-spectrum disorder. Defined as the capacity to impute states of mind to oneself and others,5454. Premack D, Woodruff G. Does chimpanzee have theory of mind?. Behav Brain Sci. 1978;4:515-26. individuals with a ToM deficit may have serious deficits in their interpersonal relationships, as the understanding of the mental state of others may guide one's own behavioral and emotional responses. In addition to social interactions, ToM deficits may lead to pragmatic language impairments, absence of pretend play and lack of empathy.1414. Happé F, Frith U. The neuropsychology of autism. Brain. 1996;119:1377-1400.

ToM may be divided into two domains: decoding mental state, which involves the capacity to perceive the mental state of others in observable information, such as facial expression and gestures; and reasoning other's mental states, which involves the capacity to integrate information in the context with information about the history of people (attitudes, knowledge, experiences) to understand their behavior.5555. Sabbagh MA, Seamans EL. Intergenerational transmission of theory-of-mind. Dev Sci. 2008;11:354-60.

Eight studies evaluated ToM in parents of individuals with autism.1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. , 3737. Bölte S, Poustka F. The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol Med. 2003;33:907-15. , 4040. Palermo MT, Pasqualetti P, Barbati G, Intelligente F, Rossini PM. Recognition of schematic facial displays of emotion in parents of children with autism. Autism. 2006;10:353-64. , 4343. Losh M, Piven J. Social-cognition and the broad autism phenotype: identifying genetically meaningful phenotypes. J Child Psychol Psychiatry. 2007;48:105-12. , 4444. Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53. , 4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.

47. Wallace S, Sebastian C, Pellicano E, Parr J, Bailey A. Face processing abilities in relatives of individuals with ASD. Autism Res. 2010;3:345-9.
- 4848. Neves Mde C, Tremeau F, Nicolato R, Lauar H, Romano-Silva MA, Correa H. Facial emotion recognition deficits in relatives of children with autism are not associated with 5HTTLPR. Rev Psiquiatr Rio Gd Sul. 2011;33:261-7. In the analysis of decoding tasks, parents of individuals with autism had more difficulties in reasoning the emotions of others' than parents in the control group in the studies conducted by Palermo et al.4040. Palermo MT, Pasqualetti P, Barbati G, Intelligente F, Rossini PM. Recognition of schematic facial displays of emotion in parents of children with autism. Autism. 2006;10:353-64. (sadness and disgust), Wallace et al.4747. Wallace S, Sebastian C, Pellicano E, Parr J, Bailey A. Face processing abilities in relatives of individuals with ASD. Autism Res. 2010;3:345-9. (fear and disgust) and Neves et al.4848. Neves Mde C, Tremeau F, Nicolato R, Lauar H, Romano-Silva MA, Correa H. Facial emotion recognition deficits in relatives of children with autism are not associated with 5HTTLPR. Rev Psiquiatr Rio Gd Sul. 2011;33:261-7. (fear, anger and happiness). However, results were similar to those found for the control groups in the studies conducted by Gokcen et al.4444. Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53. and Bölte & Poustka.3737. Bölte S, Poustka F. The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol Med. 2003;33:907-15. In the analysis of mental state reasoning tasks, parents of individuals with autism performed worse than the control group in the study conducted by Di Michele et al.1616. Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51. and Gokcen et al.4444. Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53. The instruments used in the evaluations were not the same.

Some studies evaluated parents of individuals with autism using behavioral and cognitive measures. Parents that had abnormal results in a behavioral domain (social interest) had a poorer performance in the ToM tests than parents of individuals with autism who had abnormal results in other behavioral domains, such as rigidity and language pragmatics, and parents of typically-developing children.4343. Losh M, Piven J. Social-cognition and the broad autism phenotype: identifying genetically meaningful phenotypes. J Child Psychol Psychiatry. 2007;48:105-12. , 4646. Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.

Discussion

This review investigated what traits may be part of the BAP of parents, particularly the triad of core symptoms and the major cognitive models. Although BAP is a topic of great interest for investigators in this field and numerous studies have been published (over 35), the quality of studies according to topic is low when domains are analyzed individually. Except for the language and communication domain, the one most often studied (16 studies), the mean number of studies per topic was seven. The constructs analyzed are heterogeneous, and the number of publications is even lower when an isolated sub-item is investigated, such as planning as a sub-item of executive functions. Therefore, further studies should be conducted before there is a definition of which traits are undoubtedly part of the group of BAP characteristics.

The results of the studies that evaluated behavioral characteristics in a global context are convergent, as parents of individuals with autism have more abnormal results than other groups of parents in the three domains. However, the analysis of subdomains reveals differences of opinion between authors, particularly in the inclusion of abnormal language structure use as part of the BAP.

Although they all belong to the same domain, subdomains may have different cognitive origins, and the combination of traits may lead to biased conclusions in the understanding of these disorders. For example, the third domain of the triad includes both repetitive and stereotyped mannerisms and specific and intense interests. Therefore, as the number of traits included in one single domain increases, more contradictory findings will be reported. The instruments used in the evaluation of behavioral characteristics often include several different characteristics within each domain. To ensure less discrepancy between results, future studies should use instruments that evaluate the three behavioral domains individually and include the subdomains of each factor.

The analysis of the cognitive models of autism in the literature revealed that there is a cognitive abnormality associated with each behavioral symptom and responsible for it.1515. Happé F, Ronald A, Plomin R. Time to give up on a single explanation for autism. Nat Neurosci. 2006;9:1218-20. According to some hypotheses, ToM deficits may be associated with social deficits and deficits in communication3636. Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307.; the deficits in executive functions may be associated with the high level of rigidity and perseveration5353. Hill EL. Executive dysfunction in autism. Trends Cogn Sci. 2004;8:26-32.; and weak central coherence may be associated with communication difficulties5151. 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;107:377-93. and visual and spatial differences.5050. Happé F. Autism: cognitive deficit or cognitive style? Trends Cogn Sci. 1999;3: 216-22.However, as these models are not universally adopted in autism, they are also not expected to be in the BAP. All three theories were investigated in studies that supported or refuted their inclusion in the group of BAP characteristics, and the results are, therefore, inconclusive.

Cognitive abnormalities, as well as behavioral symptoms, are also substantially heterogeneous and divided into subdomains. Therefore, an individual may have deficits in one area, but not in another. ToM involves the ability to decode and understand mental states, whereas executive functions make up a spectrum of competences, such as the capacity of organization, planning and working memory, among others. Central coherence may also be divided, as it includes both visual and verbal skills. Therefore, when a deficit in a construct is said to be part, or not, of a group of BAP characteristics, the subdomain to which it refers should be specified.

The evaluative instrument should be examined to define whether they are capable of detecting subtle changes, because the BAP is, by definition, made up of milder characteristics than those that define diagnostic criteria. For example, the block design test, which can detect superior performance in individuals with autism,5656. Ropar D, Mitchell P. Susceptibility to illusions and performance on visuospatial tasks in individuals with autism. J Child Psychol Psychiatry. 2001;42:539-49. did not detect any differences between groups of parents, which left a question open: is the test unreliable for this evaluation, or is weak central coherence actually not found in parents of individuals with autism? As the studies that used the Embedded Figures test found results with significant differences,3838. Bölte S, Poustka F. The broader cognitive phenotype of autism in parents: how specific is the tendency for local processing and executive dysfunction? J Child Psychol Psychiatry. 2006;47:639-45. , 4545. de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205. we believe that weak central coherence is, in fact, one of the endophenotypes of autism, and that the block design test is not reliable for this type of evaluation.

Most of the studies retrieved were conducted in developed countries. Of the four instruments used to evaluate behavioral characteristics, two have been translated to Portuguese: BAPQ (manuscript being prepared by authors) and AQ.5757. Autism Research Centre. Arc tests. www.autismresearchcentre.com/arc_tests. Accessed 2013 Jul 07.
www.autismresearchcentre.com/arc_tests...
However, neither has been validated for use with Brazilian populations.

One of the limitations of this review was the exclusion of studies that evaluated the BAP only in siblings. As the literature about it is extensive, it would not be possible to analyze the major traits in both groups and report all findings in a single review. Therefore, we chose to evaluate only those studies that included parents or both, parents and siblings. However, we believe that studies about the BAP in groups of siblings would bring a great contribution to the understanding of the possible BAP characteristics and would increase the number of studies for each domain.

Conclusion

Parents of individuals with autism have attenuated behavioral abnormalities in the triad of core symptoms that characterizes autism.

The evidence of participation of the cognitive theories of ToM deficit, executive functions deficit and weak central coherence in the group of characteristics of the endophenotype of autism is not conclusive. Further studies should be conducted using instruments that detect subtle cognitive abnormalities and evaluate the different subdomains of cognitive models.

References

  • 1
    American Psychiatric Association. Manual de diagnóstico e estatística das doenças mentais - 4ª edição. Porto Alegre: Artmed; 2002.
  • 2
    Wing L. The continuum of autistic characteristics. In: Schopler E, Mesibov GB, editors. Diagnosis and assessment in autism. New York: Plenum Press; 1988.
  • 3
    Klin A. Autismo e síndrome de Asperger: uma visão geral. Rev Rev Psiquiatr Rio Gd Sul. 2006;28:47-53.
  • 4
    Sucksmith E, Roth I, Hoekstra RA. Autistic traits below the clinical threshold: re-examining the broader autism phenotype in the 21st century. Neuropsychol Rev. 2011;21:360-89.
  • 5
    Gerdts J, Bernier R. The broader autism phenotype and its implications on the etiology and treatment of autism spectrum disorders. Autism Res Treat. 2011;2011:545901.
  • 6
    Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997;74:398-411.
  • 7
    Bishop DV, Maybery M, Maley A, Wong D, Hill W, Hallmayer J. Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: a study using the Autism-Spectrum Quotient. J Child Psychol Psychiatry. 2004;45:1431-6.
  • 8
    Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37:1679-90.
  • 9
    Pickles A, Starr E, Kazak S, Bolton P, Papanikolaou K, Bailey A, et al. Variable expression of the autism broader phenotype: findings from extended pedigrees J Child Psychol Psychiatry. 2000;41:491-502.
  • 10
    Scheeren AM, Stauder JE. Broader autism phenotype in parents of autistic children: reality or myth? J Autism Dev Disord. 2008;38:276-87.
  • 11
    Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ). Mol Autism. 2010;1:2-9.
  • 12
    Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636-45.
  • 13
    Viding E, Blakemore SJ. Endophenotype approach to developmental psychopathology: implications for autism research. Behav Genet. 2007;37:51-60.
  • 14
    Happé F, Frith U. The neuropsychology of autism. Brain. 1996;119:1377-1400.
  • 15
    Happé F, Ronald A, Plomin R. Time to give up on a single explanation for autism. Nat Neurosci. 2006;9:1218-20.
  • 16
    Di Michelle V, Mazza M, Cerbo R, Roncone R, Casacchia M. Deficits in pragmatic conversation as manifestation of genetic liability in autism. Clin Neuropsychiatry. 2007;4:144-51.
  • 17
    Bolton P, Macdonald H, Pickles A, Rios P, Goode S, Crowson M, et al. A case-control family history study of autism. J Child Psychol Psychiatry. 1994;35:877-900.
  • 18
    Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord. 2001;31:5-17.
  • 19
    Dawson G, Estes A, Munson J, Schellenberg G, Bernier R, Abbott R. Quantitative assessment of autism symptom-related traits in probands and parents: Broader Phenotype Autism Symptom Scale. J Autism Dev Disord. 2007;37:523-36.
  • 20
    Piven J, Palmer P, Jacobi D, Childress D, Arndt S. Broader autism phenotype: evidence from a family history study of multiple-incidence autism families. Am J Psychiatry. 1997;154:185-90.
  • 21
    Fombonne E, Bolton P, Prior J, Jordan H, Rutter M. A family study of autism: cognitive patterns and levels in parents and siblings. J Child Psychol Psychiatry. 1997;38:667-83.
  • 22
    Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, et al. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117-28.
  • 23
    Whitehouse AJ, Barry JG, Bishop DV. The broader language phenotype of autism: a comparison with specific language impairment. J Child Psychol Psychiatry. 2007;48:822-30.
  • 24
    Bernier R, Gerdts J, Munson J, Dawson G, Estes A. Evidence for the broader autism phenotype characteristics in parents from multiple-incidence families. Autism Res. 2012;5:13-20.
  • 25
    Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychol Med. 1992;22:245-54.
  • 26
    Baron-Cohen S, Bolton P, Wheelwright S, Scahill V, Short L, Mead G, et al. Autism occurs more often in families of physicists, engineers, and mathematicians. Autism. 1998;2:296-301.
  • 27
    Ruser TF, Arin D, Dowd M, Putnam S, Winklosky B, Rosen-Sheidley B, et al. Communicative competence in parents of children with autism and parents of children with specific language impairment. J Autism Dev Disord. 2007;37:1323-36.
  • 28
    Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: a comparison across parents of multiple- and single-incidence autism families. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:424-33.
  • 29
    Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC. Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008;30:557-67.
  • 30
    Lindgren KA, Folstein SE, Tomblin JB, Tager-Flusberg H. Language and reading abilities of children with autism spectrum disorders and specific language impairment and their first-degree relatives. Autism Res. 2009;2:22-38.
  • 31
    Whitehouse AJ, Coon H, Miller J, Salisbury B, Bishop DV. Narrowing the broader autism phenotype: a study using the Communication Checklist-Adult Version (CC-A). Autism. 2010;14:559-74.
  • 32
    Bishop DV, Maybery M, Wong D, Maley A, Hill W, Hallmayer J. Are phonological processing deficits part of the broad autism phenotype? Am J Med Genet B Neuropsychiatr Genet. 2004;128B:54-60.
  • 33
    Szatmari P, Georgiades S, Duku E, Zwaigenbaum L, Goldberg J, Bennett T. Alexithymia in parents of children with autism spectrum disorder. J Autism Dev Disord. 2008;38:1859-65.
  • 34
    Piven J, Palmer P. Cognitive deficits in parents from multiple-incidence autism families. J Child Psychol Psychiatry. 1997;38:1011-21.
  • 35
    Hughes C, Leboyer M, Bouvard M. Executive function in parents of children with autism. Psychol Med. 1997;27:209-20.
  • 36
    Happé F, Briskman J, Frith U. Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. J Child Psychol Psychiatry. 2001;42:299-307.
  • 37
    Bölte S, Poustka F. The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol Med. 2003;33:907-15.
  • 38
    Bölte S, Poustka F. The broader cognitive phenotype of autism in parents: how specific is the tendency for local processing and executive dysfunction? J Child Psychol Psychiatry. 2006;47:639-45.
  • 39
    de Jonge MV, Kemner C, van Engeland H. Superior disembedding performance of high-functioning individuals with autism spectrum disorders and their parents: the need for subtle measures. J Autism Dev Disord. 2006;36:677-83.
  • 40
    Palermo MT, Pasqualetti P, Barbati G, Intelligente F, Rossini PM. Recognition of schematic facial displays of emotion in parents of children with autism. Autism. 2006;10:353-64.
  • 41
    Wong D, Maybery M, Bishop DV, Maley A, Hallmayer J. Profiles of executive function in parents and siblings of individuals with autism spectrum disorders. Genes Brain Behav. 2006;5:561-76.
  • 42
    Delorme R, Goussé V, Roy I, Trandafir A, Mathieu F, Mouren-Siméoni MC, et al. Shared executive dysfunctions in unaffected relatives of patients with autism and obsessive-compulsive disorder. Eur Psychiatry. 2007;22:32-8.
  • 43
    Losh M, Piven J. Social-cognition and the broad autism phenotype: identifying genetically meaningful phenotypes. J Child Psychol Psychiatry. 2007;48:105-12.
  • 44
    Gokcen S, Bora E, Erermis S, Kesikci H, Aydin C. Theory of mind and verbal working memory deficits in parents of autistic children. Psychiatry Res. 2009;166:46-53.
  • 45
    de Jonge M, Kemner C, Naber F, van Engeland H. Block design reconstruction skills: not a good candidate for an endophenotypic marker in autism research. Eur Child Adolesc Psychiatry. 2009;18:197-205.
  • 46
    Losh M, Adolphs R, Poe MD, Couture S, Penn D, Baranek GT, et al. Neuropsychological profile of autism and the broad autism phenotype. Arch Gen Psychiatry. 2009;66:518-26.
  • 47
    Wallace S, Sebastian C, Pellicano E, Parr J, Bailey A. Face processing abilities in relatives of individuals with ASD. Autism Res. 2010;3:345-9.
  • 48
    Neves Mde C, Tremeau F, Nicolato R, Lauar H, Romano-Silva MA, Correa H. Facial emotion recognition deficits in relatives of children with autism are not associated with 5HTTLPR. Rev Psiquiatr Rio Gd Sul. 2011;33:261-7.
  • 49
    Frith U. Autism: Explaining the enigma. Oxford: Blackwell; 1989.
  • 50
    Happé F. Autism: cognitive deficit or cognitive style? Trends Cogn Sci. 1999;3: 216-22.
  • 51
    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;107:377-93.
  • 52
    Malloy-Diniz LF, Sedo M, Fuentes D, Leite WB. Neuropsicologia das funções executivas. In: Fuentes D, Malloy-Diniz L, Camargos CP, Cosenza RM, editors. Neuropsicologia: teoria e prática. Porto Alegre: Artmed; 2008.
  • 53
    Hill EL. Executive dysfunction in autism. Trends Cogn Sci. 2004;8:26-32.
  • 54
    Premack D, Woodruff G. Does chimpanzee have theory of mind?. Behav Brain Sci. 1978;4:515-26.
  • 55
    Sabbagh MA, Seamans EL. Intergenerational transmission of theory-of-mind. Dev Sci. 2008;11:354-60.
  • 56
    Ropar D, Mitchell P. Susceptibility to illusions and performance on visuospatial tasks in individuals with autism. J Child Psychol Psychiatry. 2001;42:539-49.
  • 57
    Autism Research Centre. Arc tests. www.autismresearchcentre.com/arc_tests. Accessed 2013 Jul 07.
    » www.autismresearchcentre.com/arc_tests
  • This study was part of a MSc thesis entitled "Ocorrência de fenótipo ampliado do autismo em pais de crianças portadoras da síndrome" (Occurrence of the broad autism phenotype in parents of individuals with autism), presented on June 22 2012 at the Graduate Program in Health Sciences of Instituto de Previdência dos Servidores do Estado de Minas Gerais (IPSEMG), Belo Horizonte, MG, Brazil.
  • Suggested citation: Cruz LP, Camargos-Júnior W, Rocha FL. The broad autism phenotype in parents of autistic individuals: a systematic review of the literature. Trends Psychiatry Psychother. 2013;35(4):252-263. http://dx.doi.org/10.1590/2237-6089-2013-0019

Publication Dates

  • Publication in this collection
    Dec 2013

History

  • Received
    05 May 2013
  • Accepted
    06 Aug 2013
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