Abstract
Turner syndrome (TS) is a genetic disorder, affecting 1/2500 to 1/3000 live female births, induced by partial or total deletion of one X chromosome. The neurocognitive profile of girls with TS is characterized by a normal Verbal IQ and weaknesses in visual-spatial, mathematics, and social cognitive domains. Executive functions (EFs) impairments have also been reported in these young patients. However, methodological differences across studies do not allow determination of which EFs are impaired and what is the magnitude of these impairments. The aim of this review was to clarify the EF profile of children and adolescents with TS. Sixteen samples, from thirteen studies, were included in the current meta-analysis. EFs measures used in these studies were classified into working memory, inhibitory control, cognitive flexibility, or higher-order EFs tasks in accordance with Diamond’s model, Annual Review of Psychology, 64, 135–168 (2013). Results confirmed that girls with TS had significant executive impairments with effect sizes varying from small (inhibitory control) to medium (cognitive flexibility) and large (working memory, higher-order EFs). Analyses by task revealed that cognitive inhibition may be more impaired than the other inhibitory control abilities. Heterogeneity across cognitive flexibility measures was also highlighted. Between-sample heterogeneity was observed for three tasks and the impact of participants’ characteristics on EFs was discussed. This meta-analysis confirms the necessity to assess, in patients living with TS, each EF by combining both visual and verbal tasks. Results also underline that, when studying girls with TS’ executive profile, it is important to explore the impact of moderator variables, such as IQ, parental socio-economic status, TS karyotype, psychiatric comorbidities, and hormonal treatment status.
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Acknowledgments
This work was supported by grants from the research program EnJeu[x] Enfance & Jeunesse financed by the region Pays de la Loire, France. Authors would like to thank Alexandre Laurent for his assistance in statistical analyses.
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Appendix
Appendix
Working Memory Task
Digit Span Subtest
Funnel Plot of the Digit Span Subtest
Leave-one-out method’s results:
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −0.92 | [−1.10; −0.75] | −10.38 | 0.000 | 2.01 | 0.85 | 0.00 | 0.00 |
Romans et al. 1997 (10 to 12.5) | −0.94 | [−1.11; −0.76] | −10.51 | 0.000 | 1.41 | 0.92 | 0.00 | 0.00 |
Romans et al. 1997 (12.5 to 16.9) | −0.90 | [−1.08; −0.73] | −10.09 | 0.000 | 2.04 | 0.84 | 0.00 | 0.00 |
Romans et al. 1998 | −0.91 | [−1.09; −0.73] | −9.81 | 0.000 | 2.15 | 0.83 | 0.00 | 0.00 |
Ross et al. 1995 (younger) | −0.87 | [−1.05; −0.70] | −9.86 | 0.000 | 0.76 | 0.98 | 0.00 | 0.00 |
Ross et al. 1995 (older) | −0.92 | [−1.09; −0.75] | −10.52 | 0.000 | 2.06 | 0.84 | 0.00 | 0.00 |
Rovet et al. 1994 | −0.91 | [−1.09; −0.73] | −9.84 | 0.000 | 2.15 | 0.83 | 0.00 | 0.00 |
Inhibitory Control Tasks
Matching Familiar Figures Test
Funnel Plot of the Matching Familiar Figures Test (Correct Answers)
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −0.39 | [−0.67; −0.11] | −2.74 | 0.006 | 7.96 | 0.093 | 0.05 | 49.76 |
Romans et al. 1997 (10 to 12.5) | −0.43 | [−0.66; −0.20] | −3.62 | 0.000 | 5.32 | 0.255 | 0.02 | 24.87 |
Romans et al. 1997 (12.5 to 16.9) | −0.33 | [−0.64; −0.01] | −2.05 | 0.040 | 9.86 | 0.043 | 0.08 | 59.43 |
Romans et al. 1998 | −0.25 | [−0.48; −0.01] | −2.03 | 0.042 | 5.45 | 0.244 | 0.02 | 26.62 |
Ross et al. 1995 (younger) | −0.29 | [−0.58; −0.01] | −1.92 | 0.055 | 8.70 | 0.069 | 0.06 | 54.03 |
Ross et al. 1995(older) | −0.33 | [−0.63; −0.02] | −2.11 | 0.035 | 9.85 | 0.043 | 0.07 | 59.41 |
Funnel Plot of the Matching Familiar Figures Test (Response Time Variable)
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | 0.15 | [−0.05; 0.34] | 1.44 | 0.150 | 5.85 | 0.321 | 0.01 | 14.58 |
Romans et al. 1997 (10 to 12.5) | 0.20 | [0.01; 0.38] | 2.08 | 0.038 | 3.29 | 0.656 | 0.00 | 0.00 |
Romans et al. 1997 (12.5 to 16.9) | 0.12 | [−0.08; 0.32] | 1.16 | 0.246 | 5.92 | 0.314 | 0.01 | 15.47 |
Romans et al. 1998 | 0.07 | [−0.12; 0.26] | 0.72 | 0.469 | 3.47 | 0.627 | 0.00 | 0.00 |
Ross et al. 1995 (younger) | 0.10 | [−0.09; 0.29] | 1.04 | 0.298 | 5.15 | 0.398 | 0.00 | 2.91 |
Ross et al. 1995 (older) | 0.14 | [−0.06; 0.34] | 1.37 | 0.169 | 5.97 | 0.309 | 0.01 | 16.27 |
Ross et al. 1998 | 0.16 | [−0.03; 0.35] | 1.67 | 0.095 | 5.35 | 0.375 | 0.00 | 6.51 |
Test of Variables of Attention
Funnel Plot of the Test of Variables of Attention (Commission Errors)
Leave-one-out method’s results:
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −0.49 | [−0.69; −0.29] | −4.85 | 0.000 | 3.94 | 0.414 | 0.00 | 0.00 |
Romans et al. 1997 (10 to 12.5) | −0.42 | [−0.63; −0.22] | −4.15 | 0.000 | 3.87 | 0.424 | 0.00 | 0.00 |
Romans et al. 1997 (12.5 to 16.9) | −0.49 | [−0.70; −0.29] | −4.76 | 0.000 | 4.01 | 0.405 | 0.00 | 0.28 |
Romans et al. 1998 | −0.44 | [−0.66; −0.23] | −4.01 | 0.000 | 4.41 | 0.354 | 0.01 | 9.24 |
Ross et al. 1995 (younger) | −0.50 | [−0.71; −0.30] | −4.90 | 0.000 | 3.48 | 0.480 | 0.00 | 0.00 |
Ross et al. 1995 (older) | −0.41 | [−0.60; −0.21] | −4.09 | 0.000 | 2.28 | 0.684 | 0.00 | 0.00 |
Funnel Plot of the Test of Variables of Attention (Response Time Variable)
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | 0.31 | [0.02; 0.06] | 2.38 | 0.017 | 6.74 | 0.151 | 0.03 | 40.63 |
Romans et al. 1997 (10 to 12.5) | 0.32 | [0.06; 0.59] | 2.39 | 0.017 | 6.87 | 0.143 | 0.04 | 41.79 |
Romans et al. 1997 (12.5 to 16.9) | 0.31 | [0.05; 0.57] | 2.30 | 0.021 | 6.60 | 0.158 | 0.03 | 39.42 |
Romans et al. 1998 | 0.33 | [0.06; 0.60] | 2.41 | 0.016 | 6.89 | 0.142 | 0.04 | 41.97 |
Ross et al. 1995 (younger) | 0.42 | [0.22; 0.62] | 4.08 | 0.000 | 1.53 | 0.821 | 0.00 | 0.00 |
Ross et al. 1995 (older) | 0.27 | [0.06; 0.47] | 2.52 | 0.011 | 4.53 | 0.340 | 0.01 | 11.62 |
Cognitive Flexibility Tasks
Wisconsin Card Sorting Test
Funnel Plot of the Wisconsin Card Sorting Test
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −0.21 | [−0.62; 0.20] | −1.00 | 0.314 | 7.94 | 0.047 | 0.11 | 62.22 |
Romans et al. 1997 (10 to 12.5) | −0.06 | [−0.37; 0.26] | −0.35 | 0.725 | 4.37 | 0.225 | 0.03 | 31.29 |
Romans et al. 1997 (12.5 to 16.9) | −0.30 | [−0.63; 0.03] | −1.76 | 0.079 | 4.48 | 0.214 | 0.04 | 33.00 |
Romans et al. 1998 | −0.09 | [−0.53; 0.34] | −0.43 | 0.670 | 6.88 | 0.076 | 0.11 | 56.38 |
Temple et al. 1996 | −0.22 | [−0.62; 0.18] | −1.07 | 0.283 | 7.69 | 0.053 | 0.10 | 60.98 |
Phonemic Verbal Fluency Task
Funnel Plot of the Phonemic Verbal Fluency Task
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Rae et al. 2004 | −0.81 | [−1.19; −0.42] | −4.10 | 0.000 | 14.4 | 0.025 | 0.15 | 58.49 |
Romans et al. 1997 (7 to 9.9) | −0.79 | [−1.19; −0.39] | −3.85 | 0.000 | 15.7 | 0.016 | 0.17 | 61.68 |
Romans et al. 1997 (10 to 12.5) | −0.78 | [−1.19; −0.37] | −3.73 | 0.000 | 16.3 | 0.012 | 0.18 | 63.10 |
Romans et al. 1997 (12.5 to 16.9) | −0.61 | [−1.06; −0.16] | −2.65 | 0.010 | 18.9 | 0.004 | 0.24 | 68.26 |
Romans et al. 1998 | −0.60 | [−1.08; −0.11] | −2.41 | 0.016 | 17.0 | 0.009 | 0.27 | 64.72 |
Ross et al. 2000 | −0.67 | [−1.16; −0.18] | −2.67 | 0.008 | 19.8 | 0.003 | 0.29 | 69.69 |
Temple et al. 1996 | −0.67 | [−1.14; −0.20] | −2.79 | 0.005 | 20.0 | 0.002 | 0.26 | 70.00 |
Temple 2002 | −0.58 | [−0.99; −0.16] | −2.70 | 0.007 | 15.8 | 0.015 | 0.18 | 61.99 |
Semantic Verbal Fluency Task
Funnel Plot of the Semantic Verbal Fluency Task
Leave-One-Out Method’s Results
Higher-Order Executive Function Tasks
Tower of Hanoi
Funnel Plot of the Tower of Hanoi (Score Variable)
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −0.69 | [−0.97; −0.42] | −4.93 | 0.000 | 1.77 | 0.413 | 0.00 | 0.00 |
Romans et al. 1997 (10 to 12.5) | −0.72 | [−1.02; −0.43] | −4.88 | 0.000 | 1.32 | 0.517 | 0.00 | 0.00 |
Romans et al. 1997 (12.5 to 16.9) | −0.56 | [−0.87; −0.25] | −3.59 | 0.000 | 0.58 | 0.747 | 0.00 | 0.00 |
Romans et al. 1998 | −0.66 | [−1.02; −0.30] | −3.60 | 0.000 | 2.15 | 0.341 | 0.01 | 7.05 |
Funnel Plot of the Tower of Hanoi (Average Time Variable)
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Romans et al. 1997 (7 to 9.9) | −1.00 | [−1.29; −0.72] | −6.94 | 0.000 | 1.46 | 0.482 | 0.00 | 0.00 |
Romans et al. 1997 (10 to 12.5) | −0.99 | [−1.32; −0.65] | −5.80 | 0.000 | 2.36 | 0.307 | 0.01 | 15.29 |
Romans et al. 1997 (12.5 to 16.9) | −0.84 | [−1.16; −0.53] | −5.25 | 0.000 | 1.23 | 0.542 | 0.00 | 0.00 |
Romans et al. 1998 | −0.90 | [−1.33; −0.47] | −4.10 | 0.000 | 2.84 | 0.242 | 0.04 | 29.47 |
Rey-Osterrieth Complex Figure
Funnel Plot of the Rey-Osterrieth Complex Figure
Leave-One-Out Method’s Results
Estimate | 95% [C.I.] | Z | p-value | Q | p-value | Tau2 | I2 | |
|---|---|---|---|---|---|---|---|---|
Reiss et al. 1995 | −0.98 | [−1.13; −0.83] | −12.57 | 0.000 | 4.56 | 0.601 | 0.00 | 0.00 |
Romans et al. 1997 (7 to 9.9) | −0.99 | [−1.14; −0.83] | −12.51 | 0.000 | 4.37 | 0.627 | 0.00 | 0.00 |
Romans et al. 1997 (10 to 12.5) | −0.99 | [−1.14; −0.83] | −12.46 | 0.000 | 4.41 | 0.621 | 0.00 | 0.00 |
Romans et al. 1997 (12.5 to 16.9) | −0.96 | [−1.12; −0.81] | −12.16 | 0.000 | 4.33 | 0.632 | 0.00 | 0.00 |
Romans et al. 1998 | −0.97 | [−1.13; −0.81] | −11.89 | 0.000 | 4.57 | 0.601 | 0.00 | 0.00 |
Ross et al. 1995 (younger) | −0.98 | [−1.14; −0.83] | −12.43 | 0.000 | 4.48 | 0.612 | 0.00 | 0.00 |
Ross et al. 1995 (older) | −0.94 | [−1.09; −0.78] | −12.08 | 0.000 | 0.74 | 0.993 | 0.00 | 0.00 |
Ross et al. 1997a | −1.01 | [−1.18; −0.83] | −11.36 | 0.000 | 4.17 | 0.653 | 0.00 | 0.00 |
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Mauger, C., Lancelot, C., Roy, A. et al. Executive Functions in Children and Adolescents with Turner Syndrome: A Systematic Review and Meta-Analysis. Neuropsychol Rev 28, 188–215 (2018). https://doi.org/10.1007/s11065-018-9372-x
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DOI: https://doi.org/10.1007/s11065-018-9372-x