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Published in: Acta Neurologica Belgica 3/2024

25-03-2024 | Tuberous Sclerosis | Original article

Neuropsychiatric comorbidities in tuberous sclerosis complex patients with epilepsy: results of the TAND checklist survey

Authors: Hom-Yi Lee, Chien-Heng Lin, Xing-An Wang, Jeng-Dau Tsai

Published in: Acta Neurologica Belgica | Issue 3/2024

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Abstract

Purpose

In addition to epilepsy, individuals with tuberous sclerosis complex (TSC) experience a wide range of behavioral, psychiatric, intellectual, academic, and psychosocial problems. They usually exert a large psychological burden on individuals with these illnesses.

Methods

This cross-sectional study used TSC-associated neuropsychiatric disorders (TAND) checklist interviews conducted at a single medical center. The enrollment of all subjects was > 6 years, and the comorbidities of neurodevelopmental disorders were assessed by clinical psychologists before enrollment. To assess the spectrum of TAND, the TAND checklist was applied as stated in the protocol, and the responses to the TAND checklist were evaluated by clinical psychologists.

Results

In the behavioral concerns of patients with TSC without epilepsy, those with epilepsy had excessive shyness, language delay, lack of eye contact, rigid behavior, inattentiveness, and restlessness. In psychiatric disorders, autism spectrum disorder and attention-deficit/hyperactivity disorder are significantly correlated with epilepsy history. Diminished academic skills, including reading, writing, and mathematics skills, are significantly associated with epilepsy history. For intellectual ability, TSC patients without epilepsy is associated normal intelligence level. Among neuropsychological skills, deficits in attention, dual tasking/multi-tasking, visuospatial tasking, and executive skills are significantly associated with epilepsy history.

Conclusions

Epilepsy in patients with TSC contributes to comorbid neuropsychiatric disorders. In addition to epilepsy evaluation, it is crucial to evaluate the heterogeneous spectrum of neuropsychiatric disorders using a standard checklist during the annual clinical follow-up of patients with TSC.
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Literature
1.
go back to reference Tsai JD, Ho MC, Lee HY, Shen CY, Li JY, Weng JC (2021) Disrupted white matter connectivity and organization of brain structural connectomes in tuberous sclerosis complex patients with neuropsychiatric disorders using diffusion tensor imaging. MAGMA 34:189–200CrossRefPubMed Tsai JD, Ho MC, Lee HY, Shen CY, Li JY, Weng JC (2021) Disrupted white matter connectivity and organization of brain structural connectomes in tuberous sclerosis complex patients with neuropsychiatric disorders using diffusion tensor imaging. MAGMA 34:189–200CrossRefPubMed
2.
go back to reference Kaczorowska M, Jurkiewicz E, Domańska-Pakieła D, Syczewska M, Lojszczyk B, Chmielewski D et al (2011) Cerebral tuber count and its impact on mental outcome of patients with tuberous sclerosis complex. Epilepsia 52:22–27CrossRefPubMed Kaczorowska M, Jurkiewicz E, Domańska-Pakieła D, Syczewska M, Lojszczyk B, Chmielewski D et al (2011) Cerebral tuber count and its impact on mental outcome of patients with tuberous sclerosis complex. Epilepsia 52:22–27CrossRefPubMed
4.
go back to reference Asato MR, Hardan AY (2004) Neuropsychiatric problems in tuberous sclerosis complex. J Child Neurol 19:241–249CrossRefPubMed Asato MR, Hardan AY (2004) Neuropsychiatric problems in tuberous sclerosis complex. J Child Neurol 19:241–249CrossRefPubMed
5.
go back to reference de Vries PJ, Whittemore VH, Leclezio L, Byars AW, Dunn D, Ess KC, Hook D et al (2015) Tuberous sclerosis associated neuropsychiatric disorders (TAND) and the TAND Checklist. Pediatr Neurol 52:25–35CrossRefPubMed de Vries PJ, Whittemore VH, Leclezio L, Byars AW, Dunn D, Ess KC, Hook D et al (2015) Tuberous sclerosis associated neuropsychiatric disorders (TAND) and the TAND Checklist. Pediatr Neurol 52:25–35CrossRefPubMed
6.
go back to reference Toldo I, Brasson V, Miscioscia M, Pelizza MF, Manara R, Sartori S et al (2019) Tuberous sclerosis-associated neuropsychiatric disorders: a paediatric cohort study. Dev Med Child Neurol 61:168–173CrossRefPubMed Toldo I, Brasson V, Miscioscia M, Pelizza MF, Manara R, Sartori S et al (2019) Tuberous sclerosis-associated neuropsychiatric disorders: a paediatric cohort study. Dev Med Child Neurol 61:168–173CrossRefPubMed
7.
go back to reference Kingswood JC, d’Augères GB, Belousova E, Ferreira JC, Carter T, Castellana R et al (2017) TuberOus SClerosis registry to increase disease awareness (TOSCA)—baseline data on 2093 patients. Orphanet J Rare Dis 12:2CrossRefPubMedPubMedCentral Kingswood JC, d’Augères GB, Belousova E, Ferreira JC, Carter T, Castellana R et al (2017) TuberOus SClerosis registry to increase disease awareness (TOSCA)—baseline data on 2093 patients. Orphanet J Rare Dis 12:2CrossRefPubMedPubMedCentral
8.
go back to reference Nabbout R, Belousova E, Benedik MP, Carter T, Cottin V, Curatolo P, TOSCA Consortium and TOSCA Investigators et al (2018). Epilepsy in tuberous sclerosis complex: findings from the TOSCA study. Epilepsia Open 4:73–84CrossRefPubMedPubMedCentral Nabbout R, Belousova E, Benedik MP, Carter T, Cottin V, Curatolo P, TOSCA Consortium and TOSCA Investigators et al (2018). Epilepsy in tuberous sclerosis complex: findings from the TOSCA study. Epilepsia Open 4:73–84CrossRefPubMedPubMedCentral
9.
go back to reference de Vries PJ, Hunt A, Bolton PF (2007) The psychopathologies of children and adolescents with tuberous sclerosis complex (TSC): a postal survey of UK families. Eur Child Adolesc Psychiatry 16:16–24CrossRefPubMed de Vries PJ, Hunt A, Bolton PF (2007) The psychopathologies of children and adolescents with tuberous sclerosis complex (TSC): a postal survey of UK families. Eur Child Adolesc Psychiatry 16:16–24CrossRefPubMed
10.
go back to reference Gipson TT, Johnston MV (2017) New insights into the pathogenesis and prevention of tuberous sclerosis-associated neuropsychiatric disorders (TAND). F1000Res. 6:F1000 Faculty Rev-859 Gipson TT, Johnston MV (2017) New insights into the pathogenesis and prevention of tuberous sclerosis-associated neuropsychiatric disorders (TAND). F1000Res. 6:F1000 Faculty Rev-859
11.
go back to reference Northrup H, Aronow ME, Bebin EM et al (2021) Updated international tuberous sclerosis complex diagnostic criteria and surveillance and management recommendations. Pediatr Neurol 123:50–66CrossRefPubMed Northrup H, Aronow ME, Bebin EM et al (2021) Updated international tuberous sclerosis complex diagnostic criteria and surveillance and management recommendations. Pediatr Neurol 123:50–66CrossRefPubMed
12.
go back to reference de Vries PJ, Belousova E, Benedik MP, Carter T, Cottin V, Curatolo P, TOSCA Consortium and TOSCA Investigators et al (2018) TSC-associated neuropsychiatric disorders (TAND): findings from the TOSCA natural history study. Orphanet J Rare Dis 13:157CrossRefPubMedPubMedCentral de Vries PJ, Belousova E, Benedik MP, Carter T, Cottin V, Curatolo P, TOSCA Consortium and TOSCA Investigators et al (2018) TSC-associated neuropsychiatric disorders (TAND): findings from the TOSCA natural history study. Orphanet J Rare Dis 13:157CrossRefPubMedPubMedCentral
14.
go back to reference Wong M (2008) Mechanisms of epileptogenesis in tuberous sclerosis complex and related malformations of cortical development with abnormal glioneuronal proliferation. Epilepsia 49:8–21CrossRefPubMed Wong M (2008) Mechanisms of epileptogenesis in tuberous sclerosis complex and related malformations of cortical development with abnormal glioneuronal proliferation. Epilepsia 49:8–21CrossRefPubMed
15.
go back to reference Wong AM, Wang HS, Schwartz ES, Toh CH, Zimmerman RA, Liu PL et al (2013) Cerebral diffusion tensor MR tractography in tuberous sclerosis complex: correlation with neurologic severity and tract-based spatial statistical analysis. AJNR Am J Neuroradiol 34:1829–1835CrossRefPubMedPubMedCentral Wong AM, Wang HS, Schwartz ES, Toh CH, Zimmerman RA, Liu PL et al (2013) Cerebral diffusion tensor MR tractography in tuberous sclerosis complex: correlation with neurologic severity and tract-based spatial statistical analysis. AJNR Am J Neuroradiol 34:1829–1835CrossRefPubMedPubMedCentral
16.
go back to reference Tsai JD, Ho MC, Shen CY, Weng JC (2022) Assessment of disrupted brain functional connectome in tuberous sclerosis complex using resting-state fMRI. Medicine (Baltimore) 101:e29024CrossRefPubMed Tsai JD, Ho MC, Shen CY, Weng JC (2022) Assessment of disrupted brain functional connectome in tuberous sclerosis complex using resting-state fMRI. Medicine (Baltimore) 101:e29024CrossRefPubMed
17.
go back to reference Miszewska D, Sugalska M, Jóźwiak S (2021) Risk factors associated with refractory epilepsy in patients with tuberous sclerosis complex: a systematic review. J Clin Med 10(23):5495CrossRefPubMedPubMedCentral Miszewska D, Sugalska M, Jóźwiak S (2021) Risk factors associated with refractory epilepsy in patients with tuberous sclerosis complex: a systematic review. J Clin Med 10(23):5495CrossRefPubMedPubMedCentral
19.
go back to reference Ruppe V, Dilsiz P, Reiss CS, Carlson C, Devinsky O, Zagzag D et al (2014) Developmental brain abnormalities in tuberous sclerosis complex: a comparative tissue analysis of cortical tubers and perituberal cortex. Epilepsia 55:539–550CrossRefPubMed Ruppe V, Dilsiz P, Reiss CS, Carlson C, Devinsky O, Zagzag D et al (2014) Developmental brain abnormalities in tuberous sclerosis complex: a comparative tissue analysis of cortical tubers and perituberal cortex. Epilepsia 55:539–550CrossRefPubMed
20.
go back to reference Krueger DA, Northrup H; International Tuberous Sclerosis Complex Consensus Group (2013) Tuberous sclerosis complex surveillance and management: recommendations of the 2012 international tuberous sclerosis complex consensus conference. Pediatr Neurol 49:255–265CrossRef Krueger DA, Northrup H; International Tuberous Sclerosis Complex Consensus Group (2013) Tuberous sclerosis complex surveillance and management: recommendations of the 2012 international tuberous sclerosis complex consensus conference. Pediatr Neurol 49:255–265CrossRef
21.
go back to reference Wei CC, Sheu JN, Liu JT, Yang SH, Chou IC, Tsai JD (2018) Trend of seizure remission in patients with tuberous sclerosis complex: a retrospective medical review. J Chin Med Assoc 81(8):724–728CrossRefPubMed Wei CC, Sheu JN, Liu JT, Yang SH, Chou IC, Tsai JD (2018) Trend of seizure remission in patients with tuberous sclerosis complex: a retrospective medical review. J Chin Med Assoc 81(8):724–728CrossRefPubMed
22.
go back to reference Gupta A, de Bruyn G, Tousseyn S, Krishnan B, Lagae L, Agarwal N (2020) TSC natural history database consortium. epilepsy and neurodevelopmental comorbidities in tuberous sclerosis complex: a natural history study. Pediatr Neurol 106:10–16CrossRefPubMed Gupta A, de Bruyn G, Tousseyn S, Krishnan B, Lagae L, Agarwal N (2020) TSC natural history database consortium. epilepsy and neurodevelopmental comorbidities in tuberous sclerosis complex: a natural history study. Pediatr Neurol 106:10–16CrossRefPubMed
23.
go back to reference Ding Y, Wang J, Zhou H, Li T, Zhou S, Wang Y (2021) Assessment of tuberous sclerosis-associated neuropsychiatric disorders using the MINI-KID tool: a pediatric case-control study. Orphanet J Rare Dis 16(1):181CrossRefPubMedPubMedCentral Ding Y, Wang J, Zhou H, Li T, Zhou S, Wang Y (2021) Assessment of tuberous sclerosis-associated neuropsychiatric disorders using the MINI-KID tool: a pediatric case-control study. Orphanet J Rare Dis 16(1):181CrossRefPubMedPubMedCentral
Metadata
Title
Neuropsychiatric comorbidities in tuberous sclerosis complex patients with epilepsy: results of the TAND checklist survey
Authors
Hom-Yi Lee
Chien-Heng Lin
Xing-An Wang
Jeng-Dau Tsai
Publication date
25-03-2024
Publisher
Springer International Publishing
Published in
Acta Neurologica Belgica / Issue 3/2024
Print ISSN: 0300-9009
Electronic ISSN: 2240-2993
DOI
https://doi.org/10.1007/s13760-024-02510-3

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