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Broad autism phenotype features of Chinese parents with autistic children and their associations with severity of social impairment in probands

  • Li-Juan Shi1,
  • Jian-Jun Ou1,
  • Jing-Bo Gong1, 2,
  • Su-Hong Wang1, 3,
  • Yuan-Yue Zhou1, 4,
  • Fu-Rong Zhu1,
  • Xu-Dong Liu5,
  • Jing-Ping Zhao1 and
  • Xue-Rong Luo1Email author
Contributed equally
BMC Psychiatry201515:168

https://doi.org/10.1186/s12888-015-0568-9

Received: 21 July 2014

Accepted: 16 July 2015

Published: 23 July 2015

Abstract

Background

Parents of children with autism have higher rates of broad autism phenotype (BAP) features than parents of typically developing children (TDC) in Western countries. This study was designed to examine the rate of BAP features in parents of children with autism and the relationship between parental BAP and the social impairment of their children in a Chinese sample.

Methods

A total of 299 families with autistic children and 274 families with TDC participated in this study. Parents were assessed using the Broad Autism Phenotype Questionnaire (BAPQ), which includes self-report, informant-report, and best-estimate versions. Children were assessed using the Chinese version of the Social Responsiveness Scale (SRS).

Results

Parents of children with autism were significantly more likely to have BAP features than were parents of TDC; mothers and fathers in families with autistic children had various BAP features. The total scores of the informant and best-estimate BAPQ versions for fathers were significantly associated with their children’s SRS total scores in the autism group, whereas the total scores of the three BAPQ versions for mothers were significantly associated with their children’s SRS total scores in the TDC group. In the autism group, the total SRS scores of children with “BAP present” parents (informant and best-estimate) were higher than the total SRS scores of children with“BAP absent” parents. In the TDC group, the total SRS scores of children with “BAP present” parents were higher than the total SRS scores of children with“BAP absent” parents (best-estimate).

Conclusions

Parents of autistic children were found to have higher rates of BAP than parents of TDC in a sample of Chinese parents. The BAP features of parents are associated with their children’s social functioning in both autism families and TDC families, but the patterns of the associations are different.

Keywords

Broad autism phenotype Parent Autism Social Adjustment Chinese

Background

Autism is a neurodevelopmental disorder marked by early-onset impairments in social interaction and communication, and unusually restricted, repetitive behavior and interests [1]. Autism has a strong genetic influence, with heritability estimates exceeding 80 % [2]. However, environmental risks and the gene-environment interplay in the etiology of autism are important for interpreting this heritability, which is never 100 %. Identification of autism susceptibility loci is complex and heterogeneous, with up to 1000 genes being implicated [3, 4]. Many genetic variants that are linked to autism have a high degree of pleiotropy (i.e., one gene affects more than one phenotype). To understand the genetic etiology of autism better, some researchers have turned their attention to the milder expression of autistic traits in parents or siblings of individuals with autism, which are referred to as the broad autism phenotype (BAP).

BAP is a term describing a group of mild, non-pathological social dysfunctions, communication traits, and unusual personality features that can often be found in the relatives of individuals with autism [5, 6]. Thus, BAP is thought to reflect a genetic propensity for the disorder. Studies on BAP would be helpful to identify which traits aggregate in family members and are, therefore, useful for restricting phenotypic heterogeneity to detect vulnerability genes for autism more accurately. Researchers from fields of autism genetics [7, 8] and behavioral genetics [9, 10] have strongly recommended such an approach. Prevalence estimates indicate that 14 % to 50 % of family members of individuals with autism exhibit at least one BAP feature [1113], and some studies have explored the relationship between parental BAP and child social function. Sasson et al. [14] who classified the parents of autistic probands into “BAP present” and “BAP absent,” found that children of “BAP present” parents had higher scores on the Social Communication Questionnaire (SCQ) than those of “BAP absent” parents. Similarly, Maxwell et al. [15] reported that paternal BAP scores significantly correlated with the Social Responsiveness Scale (SRS) scores of their children with autism spectrum disorder. The SCQ and the SRS are commonly used measures of autism.

Although several Western studies have examined the rate of BAP traits in parents with autistic children [1113, 15], little research has been conducted on this association in China. Cultural differences between China and Western counties might affect the rate of BAP traits in Chinese parents of children with autism. Since the parenting style and family interaction pattern in China are different from those in Western countries, these differences also might affect the association between parental BAP traits and the child’s social function. Therefore, we designed the present study to explore the rate of BAP in Chinese parents with autistic children, and to explore how parental BAP features are associated with the severity of autism symptoms in probands.

Methods

Participants

The research protocol for this study was approved by the ethics committee of the Second Xiangya Hospital, Central South University, China. Written informed consent was obtained from all the parents.

Autism families were recruited from special education schools, which provide interventions for children with autism. The families of typically developing children were randomly recruited from two kindergartens in the same city. The inclusion criteria for parents were their written consent to participate, intact families (biological parents still married and living together), with a child living with both parents. The exclusion criteria for parents were severe medical or genetic conditions, history of psychiatric disorders (e.g., autism, developmental disorder, depression, or schizophrenia) or any hearing/vision impairments (other than prescription glasses). Parents of typically developing children also had to have no history of autism or any related developmental disorders in first-degree relatives.

Children with autism had a previous DSM-IV diagnosis of autism made by a licensed clinician experienced in the assessment and diagnosis of autism. Typically developing children who were reported to have developmental disorders and related medical problems (e.g., epilepsy or head injury) were excluded.

A total of 324 families of children with autism and 354 families of typically developing children were recruited for the study from September 2012 to January 2015. Twenty-five families of autistic children and 56 families of typically developing children were excluded because of missing data. Another 24 families of typically developing children were excluded from all the analyses because the children had excessively high total raw scores on the SRS, since a child with a SRS total raw score exceeding 65 may have social problems [16]. This yielded a final sample of 299 families of autistic children and 274 families of typically developing children (Table 1).
Table 1

Demographic Information

 

PCA (n = 299)

PTC (n = 274)

t2

p value

 

Mean or N (SD or %)

Mean or N (SD or %)

  

Age of child, Months

59.60(14.89)

58.63(15.14)

−0.771

0.441

Gender of child, N (%)

  

97.10

<0.001

 Boys

258(86.3 %)

131(47.8 %)

  

 Girls

41(13.7 %)

143(52.2 %)

  

Child’s SRS total score

98.93(25.35)

43.23(11.29)

−30.532

<0.001

Age of father, Years

35.07(3.80)

34.97(3.94)

−0.318

0.751

Age of mother, Years

32.88(3.42)

32.60(3.40)

−0.973

0.331

Education of father, N (%)

  

14.610

0.001

 Primary to junior high school

29(9.7 %)

58(21.1 %)

  

 High school to some college

146(48.9 %)

116(42.4 %)

  

 Undergraduate or above

124(41.4 %)

100(36.5 %)

  

Education of mother, N (%)

  

19.522

<0.001

 Primary to junior high school

43(14.4 %)

81(29.5 %)

  

 High school to some college

139(46.5 %)

102(37.2 %)

  

 Undergraduate or above

117(39.1 %)

91(33.3 %)

  

Family income (Yuan)

  

44.487

<0.001

 Less than 30,000

57(19.1 %)

35(12.8 %)

  

 30,000-less than 50,000

93(31.1 %)

41(15 %)

  

 50,000-less than 70,000

48(16.1 %)

34(12.4 %)

  

 70,000-less than 100,000

43(14.4 %)

53(19.3 %)

  

 More than 100,000

58(19.4 %)

111(40.5 %)

  

PCA: parents of children with autism; PTC: parents of typically developing children. SRS: Social Responsiveness Scale. Sixty-three children with autism and sixty-three typically developing children who were younger than four 4 years old, were excluded from the analyses of SRS scores. Family income: according to the annual per capita income statistics published by the statistics for Hunan province in 2011.

The children ranged in age from 28 months through 155 months. There was no difference in age between the two groups (autism: M = 59.60 months; typically developing children: M = 58.63 months).

Measurement of parental BAP

The Broad Autism Phenotype Questionnaire (BAPQ) [17] was used to measure parental BAP features. It is a reliable screening tool for detecting BAP in adults, which assesses particular personality and language characteristics along three dimensions — Aloof personality, Rigid personality, and Pragmatic language. All parents were asked to complete the self-report version of the BAPQ, independently, as well as the informant version about their spouse. The BAPQ was presented to them as “The Personality and Preferences Questionnaire” in order to reduce bias associated with beliefs about autism. The validity of the Chinese version of the BAPQ was verified, with the permission of its author (Professor Joseph Piven: Department of Psychiatry, Neurodevelopmental Disorders Research Center, University of North Carolina), by translating it into Chinese, verifying the Chinese version by translating it back to English, and then comparing that version with the original version. Three sets of scores were obtained for each parent: self-report BAPQ scores, informant-report BAPQ scores, and best-estimate scores (the average of the self-report and informant-report scores). We adopted the cutoff values established by Sasson et al. [13] to reduce false positives and to optimize the diagnostic classification of the BAP.

Measurement of children’s social impairment

The Chinese version of the Social Responsiveness Scale (SRS) [16] was used to measure the social impairment of the children. The original SRS, which was developed by Constantino and colleagues in 2002 [18, 19], is a 65-item self-report or caregiver-report questionnaire for 4–18 years old children, that uses a 4-point Likert-type scale. The SRS, which was completed by the mothers in this study, can be used as a screening tool, as well as an aid for clinical diagnosis. It has subscale scores for specific symptom domains (Social awareness, Social cognition, Social communication, Social motivation, and Autistic mannerisms), and a total score that serves as an index of the severity of social deficits. A higher total SRS score indicates greater severity of social impairment. The SRS is applicable to all participants – not only those with autism – and it is not affected by intelligence, age, race, or the education level of respondents [18, 20]. The Chinese version of the SRS has fair test–retest reliability (intraclass correlations 0.751–0.852), internal consistency (Cronbach’s alpha 0.944–0.947), and convergent validity (Pearson’s correlations 0.609–0.865) [16].

Statistical analysis

Data analysis was performed using SPSS version 17. All statistical tests were 2-tailed using 0.05 as the level of statistical significance. Continuous variables are described using means and standard deviations (SD), whereas categorical variables are reported using frequencies and percentages. Between-group comparisons were performed using independent t-tests or analysis of variance (ANOVA) for continuous variables, and the Chi-square (χ2) test or Fisher’s exact probability test for categorical variables.

Multivariate analysis of variance (MANOVA) was performed to compare the BAPQ scores between the two parent groups. In this model, the dependent variables were self-report, informant-report, and best-estimate Aloof personality, Pragmatic language, and Rigidity subscales, and the total scores. The between-subject factors were group (PCA vs. PTC) and sex (father vs. mother).

Parents were then categorized as “BAP present” or “BAP absent,” based on whether the BAPQ self-report, informant-report, and best-estimates for the total score or any subscale scores exceeded the cutoff values reported by Sasson et al. (2013) [13]. Chi-square or Fisher’s tests were conducted to determine whether the frequency of BAP features of parents (i.e. the proportion of “present” cases) differed between families of autistic and typically developing children.

To determine if different BAP features co-occur more frequently in parents of children with autism than in parents of typically developing children, the dichotomized “present” scores on each of the three subscales and the total score were summed to indicate the number of BAP features a parent had: 0, 1, 2, 3, 4 (For example, a “3” indicates that a parent had three distinct BAP features.). The proportion of parents with different numbers of BAP features were compared between the groups.

Linear regression analyses were performed to examine whether the BAPQ total scores of parents were associated with the severity of social impairment (SRS) in their children. Paternal and maternal BAPQ total scores were entered in the regression model with child SRS score as the dependent variable. Independent sample t-tests were performed on the SRS total scores between children whose parents were “BAP present” or “BAP absent,” separately for the autism group and the typical development group.

Results

Parents’ ages were not significantly different between the autism group and typical development group. The education levels of the parents of children with autism were significantly higher than those of parents of typically developing children, but the family income of parents of children with autism was lower than that of parents of typically developing children (Table 1).

BAPQ scores

Descriptive data for the self-report, informant-report, and best-estimate BAPQ scores of the mothers and fathers in the PCA and PTC groups are presented in Table 2. MANOVA indicated there was a significant main effect of group on self-report, informant-report, and best-estimate Aloof personality subscales, the Pragmatic language subscales, and their total scores, with the parents of children with autism scoring higher than the PTC parents. There also was a significant main effect of sex on the informant-report Pragmatic language subscale, and the total score, and on the best-estimate Rigidity subscale, with mothers scoring higher than fathers. There was no significant interaction between group and sex on the BAPQ scores (See Table 2). Nor did the scores of fathers and mothers within PCA’s differ significantly on any of three versions of the subscales of the BAPQ (all p’s ≥0.05).
Table 2

Mean BAPQ scores of the two parental groups

 

Fathers

 

Mothers

 

F1(1, 1142)

F2(1, 1142)

F3(1, 1142)

 

PCA

PTC

PCA

PTC

Main effect

Main effect

Main effect

 

Mean (SD)

Mean (SD)

Mean (SD)

Mean (SD)

for sex

for group

for sex × group

Self-report BAPQ

       

Aloof personality

2.96(0.82)

2.74(0.74)

2.88(0.74)

2.74(0.66)

0.943

15.684**

0.93

Pragmatic language

2.53(0.72)

2.32(0.64)

2.47(0.68)

2.37(0.66)

0.002

15.848**

1.831

Rigidity personality

3.01(0.59)

3.01(0.52)

3.04(0.62)

3.08(0.51)

2.002

0.348

0.162

Total score

2.83(0.56)

2.69(0.49)

2.80(0.56)

2.73(0.48)

0.001

11.395*

1.398

Informant-report BAPQ

       

Aloof personality

2.94(0.86)

2.75(0.75)

2.96(0.77)

2.79(0.71)

0.402

14.904**

0.076

Pragmatic language

2.61(0.81)

2.38(0.70)

2.71(0.85)

2.52(0.77)

7.022*

20.013**

0.32

Rigidity personality

3.16(0.73)

3.11(0.57)

3.28(0.70)

3.25(0.59)

10.975*

1.003

0.121

Total score

2.91(0.66)

2.75(0.53)

2.98(0.61)

2.86(0.54)

7.278*

16.605**

0.254

Best-estimate BAPQ

       

Aloof personality

2.95(0.740

2.75(0.65)

2.92(0.65)

2.77(0.59)

0.031

20.27**

0.498

Pragmatic language

2.57(0.67)

2.35(0.57)

2.59(0.63)

2.45(0.62)

2.718

24.757**

1.186

Rigidity personality

3.09(0.55)

3.06(0.46)

3.16(0.54)

3.16(0.45)

8.593*

0.102

0.201

Total score

2.87(0.54)

2.72(0.43)

2.89(0.49)

2.79(0.43)

2.793

18.943**

0.917

BAPQ: Broad Autism Phenotype Questionnaire; PCA: parents of children with autism; PTC: parents of typically developing children.*p < 0.05;**p < 0.001.

BAP features frequency

Parents of children with autism had significantly higher rates of BAP features than the parents of typically developing children, except for the self-report Pragmatic language subscale and the informant-report and best-estimate Rigidity subscales for mothers, and the self-report and best-estimate Rigidity subscales and informant-estimate Aloof personality subscale for fathers (Table 3). Among the parents of children with autism, mothers had higher BAP rates than fathers (all p’s < 0.05), except for the self-report and informant-report Pragmatic language subscales, and the informant-report and best-estimate Rigidity subscales. Among parents of typically developing children, mothers had higher BAP rates than fathers (all p’s < 0.05), except for the self-report, informant-report, and best-estimate Rigidity subscales and the informant-report Pragmatic language subscale.
Table 3

Percentages of parents who met the criteria for BAP in the two parental groups

  

Fathers

     

Mothers

    
 

Numbers in PCA

Percentages in PCA (%)

Numbers in PTC

Percentages in PTC (%)

χ2

p-value

Numbers in PCA

Percentages in PCA (%)

Numbers in PTC

Percentages in PTC (%)

χ2

p-value

Self-report BAPQ

            

Aloof personality

29

9.7

11

4

7.1

0.008

60

20.1

35

12.8

5.5

0.019

Pragmatic language

56

18.7

23

8.4

12.8

<0.001

75

25.1

55

20.1

2

0.153

Rigidity personality

21

7

13

4.7

1.3

0.249

39

13

18

6.6

6.7

0.01

Total score

27

9

10

3.6

6.9

0.009

87

29.1

48

17.5

10.6

0.001

Informant-report BAPQ

            

Aloof personality

18

6

10

3.6

1.7

0.189

57

19.1

31

11.3

6.6

0.01

Pragmatic language

59

19.7

28

10.2

10

0.002

76

25.4

43

15.7

8.2

0.004

Rigidity personality

26

8.7

9

3.3

7.3

0.007

22

7.4

13

4.7

1.7

0.192

Total score

33

11

13

4.7

7.7

0.006

64

21.4

28

10.2

13.3

<0.001

Best-estimate BAPQ

            

Aloof personality

24

8

6

2.2

9.8

0.002

63

21.1

35

12.8

6.9

0.008

Pragmatic language

63

21.1

27

9.9

13.6

<0.001

97

32.4

60

21.9

8

0.005

Rigidity personality

19

6.4

8

2.9

3.8

0.053

23

7.7

12

4.4

2.7

0.098

Total score

39

13

8

2.9

19.5

<0.001

92

30.8

57

20.8

7.4

0.007

BAP: Broad Autism Phenotype; BAPQ: Broad Autism Phenotype Questionnaire; PCA: parents of children with autism; PTC: parents of typically developing children.

Co-occurrence of BAP features

Co-occurrence was examined by comparing the percentage of parents with multiple BAP features for the three versions of the BAPQ in the two parent groups (i.e., parents of children with autism and parents of typically developing children). Figure 1 shows the proportion of fathers and mothers in the autism group and the typical development group with 0 to 4 BAP features. As indicated in Fig. 1, 9.4 % of the fathers of children with autism had more than one BAP feature compared with 4.0 % of fathers of typically developing children (χ2 = 6.452, p = 0.011) on the self-report BAPQ. Moreover, 29.10 % of mothers of children with autism had more than one BAP feature in contrast to 17.5 % of mothers of typically developing children (χ2 = 10.644, p = 0.001). The parents (fathers and mothers) of children with autism also had higher rates of co-occurrence of BAP features on the other versions of the BAPQ, than parents of typically developing children (all p’s < 0.05).
Fig. 1

Proportion of PCA and PTC fathers and mothers with 0, 1, 2, 3, and 4 BAP features on the three versions of the BAPQ. BAP: Broad Autism Phenotype; BAPQ: Broad Autism Phenotype Questionnaire; PCA: parents of children with autism; PTC: parents of typically developing children

Relationship between parental BAPQ scores and children SRS total scores

Sixty-three children with autism and 63 typically developing children who were younger than four years old were excluded from this analysis because the SRS is not applicable for children under four years of age. There was no significant difference in age between the autistic (M = 64.59 months, SD = 12.46) and the typically developing children (M = 64.08 months, SD = 12.65). Children with autism had significantly higher SRS total scores (M = 98.93, SD = 25.35) than typically developing children (M = 43.23, SD = 11.29; t = −30.532, p < 0.001).

Regression analyses were conducted to examine the relationship between each BAPQ total score of each parent and their child’s SRS total score. To check whether outliers were exerting influence on the regression results, the statistics such as residuals, leverage, and Cook’s D were used. We found out that there were 21 outliers in autism group and 21 outliers in control group on self- and informant-report BAPQ. There were 23 outliers in autism group and 21 outliers in control group on best-estimate BAPQ. These outliers were excluded from this regression analysis. The results showed that fathers’ and mothers’ BAPQ total scores were significantly associated with their children’s SRS total scores (Self-report BAPQ ─ fathers: Beta = 0.157, p = 0.002; mothers: Beta = 0.194, p < 0.001; Informant-report BAPQ ─ fathers: Beta = 0.212, p < 0.001; mothers: Beta = 0.089, p = 0.084; Best-estimate BAPQ ─ fathers: Beta = 0.173, p = 0.004; mothers: Beta = 0.16, p = 0.007). To investigate the differential effects of paternal and maternal BAPQ total scores on their child’s social functioning, separate regression models were conducted for the autistic and control groups. We found that the three versions of BAPQ total scores of the mothers of children with autism were not significantly associated with their children’s SRS total scores (see Table 4), whereas the three versions of BAPQ total scores of the mothers of typically developing children were significantly associated with their children’s SRS total scores. The informant- and best-estimate BAPQ total scores of the fathers of children with autism were significantly associated with their children’s SRS total scores, whereas the self- and best-estimate BAPQ total scores of the fathers of typically developing children were not significantly associated with their children’s SRS total scores.
Table 4

Results from regression analysis predicting children’s SRS total scores from parental BAPQ total scores

 

Autism

TDC

 

Beta

t

p

Number

Beta

t

p

Number

Mother’s self-report BAPQ total scores

136

1.819

0.07

215

0.38

5.418

0.00

190

Father’s self-report BAPQ total scores

0.096

1.282

0.201

215

−0.046

−0.65

0.517

190

Mother’s informant-report BAPQ total scores

−0.032

−0.464

0.643

215

0.164

2.077

0.039

190

Father’s informant-report BAPQ total scores

0.22

3.179

0.002

215

0.196

2.477

0.014

190

Mother’s best-estimate BAPQ total scores

0.073

0.9

0.369

213

0.34

3.854

0.00

190

Father’s best-estimate BAPQ total scores

0.16

1.986

0.048

213

0.045

0.513

0.609

190

BAPQ: Broad Autism Phenotype Questionnaire; SRS: Social Responsiveness Scale; TDC: typically developing children.

Parents were classified as “BAP present” if at least one parent met the criteria for BAP in at least one domain (Aloofness personality, Pragmatic language, Rigidity, or total score). Independent samples t-tests revealed that, in the autism group, children of“BAP present” parents had higher SRS total scores for the informant-report (p = 0.034) and best-estimate BAPQ (p = 0.004) than children of“BAP absent” parents. In the typical development group, children with“BAP present” parents had higher SRS total scores for best-estimate BAPQ (p = 0.011) than children with “BAP absent” parents (Table 5).
Table 5

Mean SRS total scores in BAP absent and BAP present parents: autism and typically-developing children

Group

BAPQ version

BAP absent number

SRS BAP absent

BAP present number

SRS BAP present

t

p

Autism

Self-report

103

95.49 (24.71)

133

101.59 (25.62)

−1.845

0.066

 

Informant-report

113

95.27 (24.17)

123

102.28 (26.04)

−2.138

0.034

 

Best-estimate

105

93.66 (24.69)

131

103.15 (25.18)

−2.904

0.004

TDC

Self-report

128

42.16 (11.08)

83

44.89 (11.48)

−1.727

0.086

 

Informant-report

141

42.62 (10.94)

70

44.47 (11.95)

−1.124

0.262

 

Best-estimate

138

41.80 (11.31)

73

45.93 (10.83)

−2.559

0.011

TDC: typically developing children; BAP: broad autism phenotype; BAPQ: Broad Autism Phenotype Questionnaire; SRS: Social Responsiveness Scale.

Discussion

Both parents of children with autism in the present study had significantly higher total scores on all three versions of the BAPQ than parents of typically developing children. They also scored significantly higher on the Aloof personality and Pragmatic language subscales than parents of typically developing children. These findings are generally consistent with the earlier findings of Sasson and colleagues [13], which showed that PCA mothers and fathers had higher best-estimate scores on all the BAPQ subscales than control parents had. The current findings regarding sex differences in BAPQ scores did not support prior findings, which reported that the fathers of children with autism and males, in general, scored higher than females on BAP features [7, 14, 2124]. Mothers in the current study had significantly higher scores than fathers on the informant-report Pragmatic language and the Rigidity subscales, and total score, as well as on the best-estimate Rigidity subscale. However, the mothers and fathers of children with autism did not differ significantly on any of their BAPQ scores. Robel et al. [25], who used a French version of the Autism Spectrum Quotient (AQ) to study French samples of parents of children with autism also failed to find sex differences between parents. Further research using another measure of BAP with a sample of Chinese parents of children with autism is needed to confirm this finding.

The percentages on parents with BAP features on each subscale and version of the BAPQ in our sample ranged from 7 % to 32 % among mothers of children with autism and from 4 % to 22 % among mothers of typically developing children. By comparison, Western studies have reported that 10 %-23 % [13] and 10 %-12 % [15] of mothers of children with autism have BAP features and 4 %-10 % [13], 1 %-6 % [15] of mothers of typically developing children have BAP features. The rate of BAP features ranged between 6 % and 21 % among fathers of children with autism and between 2 % and 10 % among fathers of children with typical development. These rates are generally consistent with Western studies, which have reported that roughly 13 %-21.6 % of fathers of children with autism and 4.7 %-12.4 % of fathers of typically developing children met the criteria for BAP [13, 15]. Mothers had higher BAP rates than fathers in our PCA group, which is inconsistent with Western studies, which have reported that a larger percentage of fathers than mothers met the criteria for BAP [15, 17, 22, 26]. It is not known why the Chinese mothers have higher BAP rates, and further study is needed to determine whether cultural background leads to such discrepant rates, or whether the variation in rates are within the expected range of these BAP characteristics. The present study found parents of children with autism were more likely than parents of typically developing children to have more than one BAP feature. This finding is consistent with previous studies that reported biological parents of children with autism exhibit more BAP traits than other parents [13].

The BAP features of parents were associated with their child’s social functioning among all the study participants, but the patterns were different in the two groups of families. In the autism group, the informant-report and best-estimate BAP features of fathers were associated with their child’s social functioning, but a similar association was not found for mothers. In contrast, an association was found in the typically developing children group between the BAP features of the mothers on the three BAPQ versions and their child’s social functioning, but there was no association between the fathers’ BAP features on self-report and best-estimate BAPQ and their child’s social functioning. This finding is consistent with previous Western studies [15, 27], which found the BAP traits of fathers were associated more strongly with their autistic children’s social functioning than were the BAP traits of mothers. Autism has a strong genetic component, as indicated by the recurrence risk in families and in twin studies [28]. Previous studies have demonstrated that paternal and maternal genes are differentially expressed in offspring [29], and the differential expression is mediated by epigenetic modification [30, 31]. For example, the relative over-expression of paternal genes may drive cognition and behavior to “more demanding” phenotypes [32], as observed in Asperger syndrome [33]. Furthermore, some parent-of- origin genetic variants, such as some inherited copy-number variants [34, 35], are likely to contribute to the etiology of autism and, therefore, to lead to different effects on the phenotype of autistic children. Our findings provide evidence that the fathers of children with autism have an important influence on the severity of their child’s autistic symptoms, and suggest that the genetic transmission is different in families with and without autism. In the autism group, paternal BAP features were associated with the child’s social functioning in the informant-report and best-estimate BAPQ versions, but not in the self-report BAPQ. This may due to the fact that some fathers of children with autism lack insight into their BAP characteristics. In the typically developing children group, paternal BAP features were associated with the child’s social functioning only in the informant-report BAPQ versions, but not in the self-report and best-estimate BAPQ, which highlights the importance of using best-estimate BAPQ versions to measure parental BAP features.

Several limitations of this study should be considered when interpreting the results reported here. First, although the diagnosis of autism in the children in the study was made according to the DSM-IV, it was not confirmed by the Autism Diagnostic Observation Schedule (ADOS) [36] or the Autism Diagnostic Interview-Revised (ADI-R) [37], because these two standard diagnostic tools are not commonly used in China at present. Second, we did not obtain other important information, such as the children’s educational status and cognitive ability, or the parents’ mental and physical health status, which may affect children’s SRS scores and parental BAPQ scores. For example, previous research has reported that parents of children with autism had greater stress and depression and a lower quality of life than parents of children with other developmental disabilities [3840]. Thus, mental health status could affect the response of the parents of children with autism. Third, the total raw scores on the SRS, which usually should be converted to gender-based T-scores, were used directly for comparison in this study in the absence of Chinese norms. Fourth, we only used the BAPQ to measure the BAP features of parents, and a study conducted with another BAP measurement questionnaire is required to validate our results.

Conclusions

The current study increases our understanding of BAP and the relationship between parental BAP and children’s social functioning in a different cultural context than that of most prior research. The most striking aspects of our work are that: (1) parents of children with autism had higher BAP rates than parents of typically developing children, and that mothers had higher BAP rates than fathers in both parental groups; and (2) the patterns of association between parental BAP and children’s social impairment in autistic families is different from the pattern in families of children with typical development. The findings of our study have important implications for future genetic studies of autism, and may be applicable to some other neurodevelopmental and psychiatric disorders.

Notes

Abbreviations

BAP: 

Broad autism phenotype

BAPQ: 

Broad Autism Phenotype Questionnaire

SRS: 

Social Responsiveness Scale

SCQ: 

Social Communication Questionnaire

DSM-IV: 

The Fourth Edition of the Diagnostic and Statistical Manual of Mental Disorders

Declarations

Acknowledgements

This study was supported by the Major State Basic Research Development Program of China (973 Program, No. 2012CB517901) and the Ministry of Health Science and technology industry special fund (No. 201302002) and Hunan Graduate student research innovation project (No. CX2013B117). The authors sincerely thank all participating children and their parents.

Authors’ Affiliations

(1)
Mental Health Institute of the Second Xiangya Hospital and Key Laboratory of Psychiatry and Mental Health of Hunan Province, The Central South University
(2)
Traditional Chinese Medicine University of Hunan
(3)
Department of Neuroscience, The Third Affiliated Hospital of Soochow University
(4)
Hangzhou Seventh People’s Hospital
(5)
Department of Psychiatry, Queen’s University

References

  1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders: 4th edn., text revision (DSM-IV-TR). Washington, DC. American Psychiatric Publishing; 2000.Google Scholar
  2. Ronald A, Hoekstra RA. Autism spectrum disorders and autistic traits: a decade of new twin studies. American journal of medical genetics Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics. 2011;156B(3):255–74.View ArticleGoogle Scholar
  3. Murdoch JD, State MW. Recent developments in the genetics of autism spectrum disorders. Curr Opin Genet Dev. 2013;23(3):310–5.View ArticlePubMedGoogle Scholar
  4. Geschwind DH. Genetics of autism spectrum disorders. Trends Cogn Sci. 2011;15(9):409–16.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Constantino JN, Lajonchere C, Lutz M, Gray T, Abbacchi A, McKenna K, et al. Autistic social impairment in the siblings of children with pervasive developmental disorders. Am J Psychiatry. 2006;163(2):294–6.View ArticlePubMedGoogle Scholar
  6. Rutter M. Genetic studies of autism: from the 1970s into the millennium. J Abnorm Child Psychol. 2000;28(1):3–14.View ArticlePubMedGoogle Scholar
  7. Smith CJ, Lang CM, Kryzak L, Reichenberg A, Hollander E, Silverman JM. Familial associations of intense preoccupations, an empirical factor of the restricted, repetitive behaviors and interests domain of autism. J Child Psychol Psychiatry. 2009;50(8):982–90.View ArticlePubMedGoogle Scholar
  8. Weiss LA. Autism genetics: emerging data from genome-wide copy-number and single nucleotide polymorphism scans. Expert Rev Mol Diagn. 2009;9(8):795–803.View ArticlePubMedGoogle Scholar
  9. de Geus EJ. Introducing genetic psychophysiology. Biol Psychol. 2002;61(1–2):1–10.View ArticlePubMedGoogle Scholar
  10. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160(4):636–45.View ArticlePubMedGoogle Scholar
  11. 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(5):877–900.View ArticlePubMedGoogle Scholar
  12. 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(3):523–36.View ArticlePubMedGoogle Scholar
  13. Sasson NJ, Lam KS, Childress D, Parlier M, Daniels JL, Piven J. The broad autism phenotype questionnaire: prevalence and diagnostic classification. Autism research : official journal of the International Society for Autism Research. 2013;6(2):134–43.View ArticleGoogle Scholar
  14. Sasson NJ, Lam KS, Parlier M, Daniels JL, Piven J. Autism and the broad autism phenotype: familial patterns and intergenerational transmission. J Neurodev Disord. 2013;5(1):11.View ArticlePubMedPubMed CentralGoogle Scholar
  15. Maxwell CR, Parish-Morris J, Hsin O, Bush JC, Schultz RT. The broad autism phenotype predicts child functioning in autism spectrum disorders. J Neurodev Disord. 2013;5(1):25.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Gau SS-F, Liu L-T, Wu Y-Y, Chiu Y-N, Tsai W-C. Psychometric properties of the Chinese version of the social responsiveness scale. Research in autism spectrum disorders. 2013;7(2):349–60.View ArticleGoogle Scholar
  17. Hurley RS, Losh M, Parlier M, Reznick JS, Piven J. The broad autism phenotype questionnaire. J Autism Dev Disord. 2007;37(9):1679–90.View ArticlePubMedGoogle Scholar
  18. Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, et al. Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord. 2003;33(4):427–33.View ArticlePubMedGoogle Scholar
  19. Constantino JN, Hudziak JJ, Todd RD. Deficits in reciprocal social behavior in male twins: evidence for a genetically independent domain of psychopathology. J Am Acad Child Adolesc Psychiatry. 2003;42(4):458–67.View ArticlePubMedGoogle Scholar
  20. Reiersen AM, Constantino JN, Volk HE, Todd RD. Autistic traits in a population-based ADHD twin sample. J Child Psychol Psychiatry. 2007;48(5):464–72.View ArticlePubMedGoogle Scholar
  21. Seidman I, Yirmiya N, Milshtein S, Ebstein RP, Levi S. The Broad Autism Phenotype Questionnaire: mothers versus fathers of children with an autism spectrum disorder. J Autism Dev Disord. 2012;42(5):837–46.View ArticlePubMedGoogle Scholar
  22. 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). Molecular autism. 2010;1(1):10.View ArticlePubMedPubMed CentralGoogle Scholar
  23. 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(8):1431–6.View ArticlePubMedGoogle Scholar
  24. Murphy M, Bolton PF, Pickles A, Fombonne E, Piven J, Rutter M. Personality traits of the relatives of autistic probands. Psychol Med. 2000;30(6):1411–24.View ArticlePubMedGoogle Scholar
  25. Robel L, Rousselot-Pailley B, Fortin C, Levy-Rueff M, Golse B, Falissard B. Subthreshold traits of the broad autistic spectrum are distributed across different subgroups in parents, but not siblings, of probands with autism. Eur Child Adolesc Psychiatry. 2014;23(4):225–33.View ArticlePubMedGoogle Scholar
  26. Davidson J, Goin-Kochel RP, Green-Snyder LA, Hundley RJ, Warren Z, Peters SU. Expression of the broad autism phenotype in simplex autism families from the Simons Simplex Collection. J Autism Dev Disord. 2014;44(10):2392–2399. Google Scholar
  27. Klusek J, Losh M, Martin GE. Sex differences and within-family associations in the broad autism phenotype. Autism : the international journal of research and practice. 2014;18(2):106–16.View ArticleGoogle Scholar
  28. Devlin B, Scherer SW. Genetic architecture in autism spectrum disorder. Curr Opin Genet Dev. 2012;22(3):229–37.View ArticlePubMedGoogle Scholar
  29. Day T, Bonduriansky R. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics. 2004;167(4):1537–46.View ArticlePubMedPubMed CentralGoogle Scholar
  30. de la Casa-Esperón E, Sapienza C. Natural selection and the evolution of genome imprinting. Annu Rev Genet. 2003;37(1):349–70.View ArticlePubMedGoogle Scholar
  31. Flashner BM, Russo ME, Boileau JE, Leong DW, Gallicano GI. Epigenetic factors and autism spectrum disorders. Neuromolecular Med. 2013;15(2):339–50.View ArticlePubMedGoogle Scholar
  32. Haig D. Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet. 2004;38:553–85.View ArticlePubMedGoogle Scholar
  33. Baron-Cohen S, Belmonte MK. Autism: a window onto the development of the social and the analytic brain. Annu Rev Neurosci. 2005;28:109–26.View ArticlePubMedGoogle Scholar
  34. Delahanty RJ, Kang J, Brune CW, Kistner EO, Courchesne E, Cox NJ, et al. Maternal transmission of a rare GABRB3 signal peptide variant is associated with autism. Mol Psychiatry. 2011;16(1):86–96.View ArticlePubMedGoogle Scholar
  35. Girirajan S, Rosenfeld JA, Coe BP, Parikh S, Friedman N, Goldstein A, et al. Phenotypic heterogeneity of genomic disorders and rare copy-number variants. N Engl J Med. 2012;367(14):1321–31.View ArticlePubMedPubMed CentralGoogle Scholar
  36. Lord C, Risi S, Lambrecht L, Cook Jr EH, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205–23.View ArticlePubMedGoogle Scholar
  37. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659–85.View ArticlePubMedGoogle Scholar
  38. Sanders JL, Morgan SB. Family stress and adjustment as perceived by parents of children with autism or Down syndrome: Implications for intervention. Child & Family Behavior Therapy. 1997;19(4):15–32.View ArticleGoogle Scholar
  39. Dabrowska A, Pisula E. Parenting stress and coping styles in mothers and fathers of pre‐school children with autism and Down syndrome. J Intellect Disabil Res. 2010;54(3):266–80.View ArticlePubMedGoogle Scholar
  40. Olsson MB, Hwang C. Depression in mothers and fathers of children with intellectual disability. J Intellect Disabil Res. 2001;45(6):535–43.View ArticlePubMedGoogle Scholar

Copyright

© Shi et al. 2015

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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