Behavioral phenotypes of pediatric temporal lobe epilepsy.
Behavior Assessment System for Children
behavioral taxonomy
cluster analysis
comorbidity
psychopathology
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
01
02
2022
received:
04
11
2021
accepted:
01
02
2022
pubmed:
18
2
2022
medline:
10
5
2022
entrez:
17
2
2022
Statut:
ppublish
Résumé
A broad spectrum of emotional-behavioral problems have been reported in pediatric temporal lobe epilepsy (TLE), but with considerable variability in their presence and nature of expression, which hampers precise identification and treatment. The present study aimed to empirically identify latent patterns or behavioral phenotypes and their correlates. Data included parental ratings of emotional-behavioral status on the Behavior Assessment System for Children, 2nd Edition (BASC-2) of 81 children (mean age = 11.79, standard deviation [SD] = 3.93) with TLE. The nine clinical subscales were subjected to unsupervised machine learning to identify behavioral subgroups. To explore concurrent validity and the underlying composition of the identified clusters, we examined demographic factors, seizure characteristics, psychosocial factors, neuropsychological performance, psychiatric status, and health-related quality of life (HRQoL). Three behavioral phenotypes were identified, which included no behavioral concerns (Cluster 1, 43% of sample), externalizing problems (Cluster 2, 41% of sample), and internalizing problems (Cluster 3, 16% of sample). Behavioral phenotypes were characterized by important differences across clinical seizure variables, psychosocial/familial factors, everyday executive functioning, and HRQoL. Cluster 2 was associated with younger child age, lower maternal education, and higher rate of single-parent households. Cluster 3 was associated with older age at epilepsy onset and higher rates of hippocampal sclerosis and parental psychiatric history. Both Cluster 2 and 3 demonstrated elevated family stress. Concurrent validity was demonstrated through the association of psychiatric (i.e., rate of Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5) disorders and psychotropic medication) and parent-rated HRQoL variables. Youth with TLE present with three distinct behavioral phenotypes that correspond with important clinical and sociodemographic markers. The current findings demonstrate the variability of behavioral presentations in youth with TLE and provide a preliminary framework for screening and targeting intervention to enhance support for youth with TLE and their families.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1177-1188Informations de copyright
© 2022 International League Against Epilepsy.
Références
Austin JK, Caplan R. Behavioral and psychiatric comorbidities in pediatric epilepsy: toward an integrative model. Epilepsia. 2007;48(9):1639-51. https://doi.org/10.1111/j.1528-1167.2007.01154.x
Ekinci O, Titus JB, Rodopman AA, Berkem M, Trevathan E. Depression and anxiety in children and adolescents with epilepsy: prevalence, risk factors, and treatment. Epilepsy Behav. 2009;14(1):8-18. https://doi.org/10.1016/j.yebeh.2008.08.015
Reilly C, Atkinson P, Das KB, Chin RFMC, Aylett SE, Burch V, et al. Neurobehavioral comorbidities in children with active epilepsy: a population-based study. Pediatrics. 2014;133(6):e1586-93. https://doi.org/10.1542/peds.2013-3787
Rodenburg R, Stams GJ, Meijer AM, Aldenkamp AP, Deković M. Psychopathology in children with epilepsy: a meta-analysis. J Pediatr Psychol. 2005;30(6):453-68. https://doi.org/10.1093/jpepsy/jsi071
Smith AW, Mara CA, Modi AC. Adherence to antiepileptic drugs in adolescents with epilepsy. Epilepsy Behav. 2018;80:307-11.
Puka K, Smith ML, Moineddin R, Snead OC, Widjaja E. The influence of socioeconomic status on health resource utilization in pediatric epilepsy in a universal health insurance system. Epilepsia. 2016;57(3):455-63.
Kanner AM, Barry JJ, Gilliam F, Hermann B, Meador KJ. Depressive and anxiety disorders in epilepsy: do they differ in their potential to worsen common antiepileptic drug-related adverse events? Epilepsia. 2012;53(6):1104-8.
Christensen J, Vestergaard M, Mortensen PB, Sidenius P, Agerbo E. Epilepsy and risk of suicide: a population-based case-control study. Lancet Neurol. 2007;6(8):693-8. https://doi.org/10.1016/S1474-4422(07)70175-8
Sillanpää M, Jalava M, Kaleva O, Shinnar S. Long-term prognosis of seizures with onset in childhood. N Engl J Med. 1998;338(24):1715-22. https://doi.org/10.1056/NEJM199806113382402
Asato MR, Caplan R, Hermann BP. Epilepsy and comorbidities-what are we waiting for? Epilepsy Behav. 2014;31:127-8. https://doi.org/10.1016/j.yebeh.2013.11.027
Wiebe S. Epidemiology of temporal lobe epilepsy. Can J Neurol Sci. 2000;27(S1):S6-10. https://doi.org/10.1017/S0317167100000561
Vinti V, Dell'Isola GB, Tascini G, Mencaroni E, Cara GD, Striano P, et al. Temporal lobe epilepsy and psychiatric comorbidity. Front Neurol. 2021;12:775781. https://doi.org/10.3389/fneur.2021.775781
Salpekar JA, Berl MM, Havens K, Cushner-Weinstein S, Conry JA, Pearl PL, et al. Psychiatric symptoms in children prior to epilepsy surgery differ according to suspected seizure focus. Epilepsia. 2013;54(6):1074-82.
Schraegle WA, Nussbaum NL, Titus JB. Executive dysfunction and depression in pediatric temporal lobe epilepsy: the contribution of hippocampal sclerosis and psychosocial factors. J Int Neuropsychol Soc. 2018;24(6):606-16. https://doi.org/10.1017/S1355617718000140
Schraegle WA, Titus JB. The relationship of seizure focus with depression, anxiety, and health-related quality of life in children and adolescents with epilepsy. Epilepsy Behav. 2017;68:115-22. https://doi.org/10.1016/j.yebeh.2016.12.009
McLellan A, Davies S, Heyman I, Harding B, Harkness W, Taylor D, et al. Psychopathology in children with epilepsy before and after temporal lobe resection. Dev Med Child Neurol. 2005;47(10):666-72. https://doi.org/10.1111/j.1469-8749.2005.tb01051.x
Dunn DW, Kronenberger WG. Childhood epilepsy, attention problems, and ADHD: review and practical considerations. Semin Peadiatr Neurol. 2005;12(4):222-8. https://doi.org/10.1016/j.spen.2005.12.004
Pereira A, Valente KD. Severity of depressive symptomatology and functional impairment in children and adolescents with temporal lobe epilepsy. Seizure. 2013;22(9):708-12. https://doi.org/10.1016/j.seizure.2013.05.008
Andrade-Machado R, Ochoa-Urrea M, Garcia-Espinosa A, Benjumea-Cuartas V, Santos-Santos A. Suicidal risk, affective dysphoric disorders, and quality-of-life perception in patients with focal refractory epilepsy. Epilepsy Behav. 2015;45:254-60. https://doi.org/10.1016/j.yebeh.2015.01.005
Park SJ, Lee HB, Ahn MH, Park S, Choi EJ, Lee HJ, et al. Identifying clinical correlates for suicide among epilepsy patients in South Korea: a case-control study. Epilepsia. 2015;56(12):1966-72. https://doi.org/10.1111/epi.13226
Hermann BP, Struck AF, Busch RM, Reyes A, Kaestner E, McDonald CR. Neurobehavioural comorbidities of epilepsy: towards a network-based precision taxonomy. Nat Rev Neurol. 2021;17(12):731-46. https://doi.org/10.1038/s41582-021-00555-z
Hermann B, Seidenberg M, Lee EJ, Chan F, Rutecki P. Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc. 2007;13(1):12-20. https://doi.org/10.1017/S135561770707004X
Elverman KH, Resch ZJ, Quasney EE, Sabsevitz DS, Binder JR, Swanson SJ. Temporal lobe epilepsy is associated with distinct cognitive phenotypes. Epilepsy Behav. 2019;96:61-8. https://doi.org/10.1016/j.yebeh.2019.04.015
Reyes A, Kaestner E, Ferguson L, Jones JE, Seidenberg M, Barr WB, et al. Cognitive phenotypes in temporal lobe epilepsy utilizing data- and clinically driven approaches: moving toward a new taxonomy. Epilepsia. 2020;61(6):1211-20. https://doi.org/10.1111/epi.16528
Baxendale S, Thompson P. The association of cognitive phenotypes with postoperative outcomes after epilepsy surgery in patients with temporal lobe epilepsy. Epilepsy Behav. 2020;112:107386. https://doi.org/10.1016/j.yebeh.2020.107386
Hermann B, Conant LL, Cook CJ, Hwang G, Garcia-Ramos C, Dabbs K, et al. Network, clinical and sociodemographic features of cognitive phenotypes in temporal lobe epilepsy. Neuroimage Clin. 2020;27:102341. https://doi.org/10.1016/j.nicl.2020.102341
Schraegle WA, Nussbaum NL, DeLeon RC, Titus JB. Neuropsychological phenotypes in pediatric temporal lobe epilepsy. J Int Neuropsychol Soc. 2021;1-10. https://doi.org/10.1017/S1355617721001090
Hermann BP, Struck AF, Stafstrom CE, Hsu DA, Dabbs K, Gundlach C, et al. Behavioral phenotypes of childhood idiopathic epilepsies. Epilepsia. 2020;61(7):1427-37. https://doi.org/10.1111/epi.16569
Hermann BP, Struck AF, Dabbs K, Seidenberg M, Jones JE. Behavioral phenotypes of temporal lobe epilepsy. Epilepsia Open. 2021;6(2):369-80. https://doi.org/10.1002/epi4.12488
Dagar A, Falcone T. Psychiatric comorbidities in pediatric epilepsy. Curr Psychiatry Rep. 2020;22(12):77. https://doi.org/10.1007/s11920-020-01195-8
Engel J. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia. 2001;42(6):796-803. https://doi.org/10.1046/j.1528-1157.2001.10401.x
Reynolds C, Kamphaus R. BASC-2: Behavioral Assessment System for Children Manual, 2nd edn. Pearson; 2004.
Holmbeck GN, Thill AW, Bachanas P, Garber J, Miller KB, Abad M, et al. Evidence-based assessment in pediatric psychology: measures of psychosocial adjustment and psychopathology. J Pediatr Psychol. 2008;33(9):958-80. https://doi.org/10.1093/jpepsy/jsm059
Allison Bender H, Auciello D, Morrison CE, MacAllister WS, Zaroff CM. Comparing the convergent validity and clinical utility of the Behavior Assessment System for Children-Parent Rating Scales and Child Behavior Checklist in children with epilepsy. Epilepsy Behav. 2008;13(1):237-42. https://doi.org/10.1016/j.yebeh.2008.03.007
Sabaz M, Cairns DR, Lawson JA, Nheu N, Bleasel AF, Bye AM. Validation of a new quality of life measure for children with epilepsy. Epilepsia. 2000;41(6):765-74.
Murtagh F, Legendre P. Ward's hierarchical agglomerative clustering method: which algorithms implement ward's criterion? J Classif. 2014;31(3):274-95. https://doi.org/10.1007/s00357-014-9161-z
Milligan GW, Hirtle SC. Clustering and classification methods. In Irving B, W, John A, S, Wayne F, V, editors. Handbook of psychology: research methods in psychology. Vol. 2, 2nd ed. John Wiley & Sons, Inc.; 2013:189-210.
Milligan GW, Cooper MC. Methodology review: clustering methods. Appl Psychol Meas. 1987;11(4):329-54. https://doi.org/10.1177/014662168701100401
Berven NL, Hubert LJ. Complete-link clustering as a complement to factor analysis: a comparison to factor analysis used alone. J Vocat Behav. 1977;10(1):69-81. https://doi.org/10.1016/0001-8791(77)90043-4
Carson J, Weir A, Chin RF, McLellan A. Socioeconomic deprivation is an independent risk factor for behavioral problems in children with epilepsy. Epilepsy Behav. 2015;45:105-9. https://doi.org/10.1016/j.yebeh.2015.03.009
Austin JK, Dunn DW. Children with epilepsy: quality of life and psychosocial needs. Annu Rev Nurs Res. 2000;18:26-47.
Puka K, Ferro MA, Anderson KK, Speechley KN. Prevalence and trajectories of depressive symptoms among mothers of children with newly diagnosed epilepsy: a longitudinal 10-year study. Epilepsia. 2019;60(2):358-66. https://doi.org/10.1111/epi.14638
McLaughlin RM, Schraegle WA, Nussbaum NL, Titus JB. Parental coping and its role in predicting health-related quality of life in pediatric epilepsy. Epilepsy Behav. 2018;87:1-6. https://doi.org/10.1016/j.yebeh.2018.08.009
Michaelis R, Tang V, Goldstein LH, Reuber M, LaFrance WC, Lundgren T, et al. Psychological treatments for adults and children with epilepsy: evidence-based recommendations by the International League Against Epilepsy Psychology Task Force. Epilepsia. 2018;59(7):1282-302. https://doi.org/10.1111/epi.14444
Modi AC, Gutierrez-Colina AM, Wagner JL, Smith G, Junger K, Huszti H, et al. Executive functioning phenotypes in youth with epilepsy. Epilepsy Behav. 2019;90:112-8. https://doi.org/10.1016/j.yebeh.2018.11.026
Eom S, Caplan R, Berg AT. Behavioral problems and childhood epilepsy: parent vs child perspectives. J Pediatr. 2016;179:233-239.e5. https://doi.org/10.1016/j.jpeds.2016.08.096
Dabbs K, Jones JE, Jackson DC, Seidenberg M, Hermann BP. Patterns of cortical thickness and the child behavior checklist in childhood epilepsy. Epilepsy Behav. 2013;29(1):198-204. https://doi.org/10.1016/j.yebeh.2013.07.008