Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-17T13:01:08.592Z Has data issue: false hasContentIssue false
  • English
  • Français

Cognitive Outcome in Childhood-Onset Epilepsy: A Five-Decade Prospective Cohort Study

Published online by Cambridge University Press:  10 January 2017

Mira Karrasch ,
Petri Tiitta ,
Bruce Hermann ,
Juho Joutsa ,
Shlomo Shinnar ,
Juha Rinne ,
Anu Anttinen  and
Matti Sillanpää
Mira Karrasch*
Affiliation:
Department of Psychology, Åbo Akademi University, Turku, Finland
Petri Tiitta
Affiliation:
Department of Public Health, University of Turku, Finland Turku Teacher Training College, University of Turku, Finland
Bruce Hermann
Affiliation:
Department of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Juho Joutsa
Affiliation:
Turku PET Centre, University of Turku and Turku University Hospital, Finland Department of Clinical Neurophysiology, University of Turku and Turku University Hospital, Finland Departments of Neurology, Pediatrics and Epidemiology and Population Health, Montefiore Medical Center, Albert Einstein College of Medicine, New York
Shlomo Shinnar
Affiliation:
Division of Clinical Neurosciences, University of Turku and Turku University Hospital, Finland
Juha Rinne
Affiliation:
Turku PET Centre, University of Turku and Turku University Hospital, Finland Department of Clinical Neurophysiology, University of Turku and Turku University Hospital, Finland
Anu Anttinen
Affiliation:
Department of Clinical Neurophysiology, University of Turku and Turku University Hospital, Finland
Matti Sillanpää
Affiliation:
Departments of Public Health and Child Neurology, University of Turku, Finland
*
Correspondence and reprint requests to: Mira Karrasch, Department of Psychology, Abo Akademi University, FIN-20500 Turku, Finland. E-mail: mira.karrasch@abo.fi.
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Little is known about the very long-term cognitive outcome in patients with childhood-onset epilepsy. The aim of this unique prospective population-based cohort study was to examine cognitive outcomes in aging participants with childhood-onset epilepsy (mean onset age=5.3 years) five decades later (mean age at follow-up=56.5 years).Methods: The sample consisted of 48 participants with childhood-onset epilepsy and 48 age-matched healthy controls aged 48–63 years. Thirty-six epilepsy participants were in remission and 12 continued to have seizures. Cognitive function was examined with 11 neuropsychological tests measuring language and semantic function, episodic memory, and learning, visuomotor function, executive function, and working memory. Results: The risk of cognitive impairment was very high in participants with continuing seizures; odds ratio (OR)=11.7 (95% confidence interval [CI] (2.8, 49.6), p=.0008). They exhibited worse performances across measures of language and semantic function, and visuomotor function compared to participants with remitted epilepsy and healthy controls. In the participants with remitted epilepsy, the risk of cognitive impairment was somewhat elevated, but not statistically significant; OR=2.6 (95% CI [0.9, 7.5], p=.08).Conclusions: Our results showed that the distinction of continued versus discontinued seizures was critical for determining long-term cognitive outcome in childhood-onset epilepsy. Few participants in remission exhibited marked cognitive impairment compared to age-matched peers. However, a subgroup of participants with decades long active epilepsy, continuous seizure activity and anti-epileptic drug (AED) medication, showed clinically significant cognitive impairment and are thus in a more precarious position when entering older age. (JINS, 2017, 23, 332–340)

Keywords

AgingLanguageNeuropsychologySeizureSemantic functionVisuomotor function
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 4 , April 2017 , pp. 332 - 340
Copyright
Copyright © The International Neuropsychological Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Äikiä, M., Salmenperä, T., Partanen, K., & Kälviäinen, R. (2001). Verbal memory in newly diagnosed patients and patients with chronic left temporal lobe epilepsy. Epilepsy & Behavior, 2(1), 20–27.CrossRefGoogle ScholarPubMed
Baxendale, S., Thompson, P.J., & Duncan, J.S. (2012). Neuropsychological function in patients who have had epilepsy surgery: A long-term follow-up. Epilepsy & Behavior, 23(1), 24–29.CrossRefGoogle ScholarPubMed
Beghi, E., Camfield, P.R., & Camfield, C.S. (2014). Epidemiologic aspects: Lost in transition. Epilepsia, 55(Suppl 3), 3–7.CrossRefGoogle ScholarPubMed
Benton, A.L., & Hamsher, K. (1976). Multilingual aphasia examination. Iowa City: University of Iowa.Google Scholar
Berg, A.T., Zelko, F.A., Levy, S.R., & Testa, F.M. (2012). Age at onset of epilepsy, pharmacoresistance, and cognitive outcomes: A prospective cohort study. Neurology, 79(13), 1384–1391.CrossRefGoogle ScholarPubMed
Bäckman, L., Jones, S., Berger, A.K., Laukka, E.J., & Small, B.J. (2005). Cognitive impairment in preclinical Alzheimer’s disease: A meta-analysis. Neuropsychology, 19(4), 520–531.CrossRefGoogle ScholarPubMed
Camfield, P.R., & Camfield, C.S. (2014). What happens to children with epilepsy when they become adults? Some facts and opinions. Pediatric Neurology, 51(1), 17–23.CrossRefGoogle ScholarPubMed
Commission on Revised Classification of Seizures. (1981). Proposal for revised clinical and electroencephalographic classification of epileptic seizures. From the Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia, 22(4), 489–501.CrossRefGoogle Scholar
Dodrill, C.B. (2004). Neuropsychological effects of seizures. Epilepsy & Behavior, 5(Suppl 1), S21–S24.CrossRefGoogle ScholarPubMed
Elger, C.E., Helmstaedter, C., & Kurthen, M. (2004). Chronic epilepsy and cognition. Lancet Neurology, 3(11), 663–672.CrossRefGoogle ScholarPubMed
Farwell, J.R., Dodrill, C.B., & Batzel, L.W. (1985). Neuropsychological abilities of children with epilepsy. Epilepsia, 26(5), 395–400.CrossRefGoogle ScholarPubMed
Fastenau, P.S., Johnson, C.S., Perkins, S.M., Byars, A.W., deGrauw, T.J., Austin, J.K., & Dunn, D.W. (2009). Neuropsychological status at seizure onset in children: Risk factors for early cognitive deficits. Neurology, 73(7), 526–534.CrossRefGoogle ScholarPubMed
Guidelines for Epidemiologic Studies on Epilepsy. (1993). Guidelines for epidemiologic studies on epilepsy. Commission on Epidemiology and Prognosis, International League Against Epilepsy. Epilepsia, 34(4), 592–596.CrossRefGoogle Scholar
Hamiwka, L.D., & Wirrell, E.C. (2009). Comorbidities in pediatric epilepsy: Beyond "just’' treating the seizures. Journal of Child Neurology, 24(6), 734–742.CrossRefGoogle ScholarPubMed
Helmstaedter, C., & Elger, C.E. (2009). Chronic temporal lobe epilepsy: A neurodevelopmental or progressively dementing disease? Brain, 132(Pt 10), 2822–2830.CrossRefGoogle ScholarPubMed
Hermann, B., Meador, K.J., Gaillard, W.D., & Cramer, J.A. (2010). Cognition across the lifespan: Antiepileptic drugs, epilepsy, or both? Epilepsy & Behavior, 17(1), 1–5.CrossRefGoogle ScholarPubMed
Hermann, B., Seidenberg, M., Bell, B., Rutecki, P, Sheth, R., Ruggles, K., & Magnotta, V. (2002). The neurodevelopmental impact of childhood-onset temporal lobe epilepsy on brain structure and function. Epilepsia, 43(9), 1062–1071.CrossRefGoogle ScholarPubMed
Hermann, B.P., Seidenberg, M., Dow, C., Jones, J., Rutecki, P., Bhattacharya, A., & & Bell, B.(2006). Cognitive prognosis in chronic temporal lobe epilepsy. Annals of Neurology, 60(1), 80–87.CrossRefGoogle ScholarPubMed
Hermann, B.P., Lin, J.J., Jones, J.E., & Seidenberg, M. (2009). The emerging architecture of neuropsychological impairment in epilepsy. Neurologic Clinics, 27(4), 881–907.CrossRefGoogle ScholarPubMed
Hommet, C., Sauerwein, H.C., De Toffol, B., & Lassonde, M. (2006). Idiopathic epileptic syndromes and cognition. Neuroscience & Biobehavioral Reviews, 30(1), 85–96.CrossRefGoogle ScholarPubMed
Ingraham, L.J., & Aiken, C.B. (1996). An empirical approach to determining criteria for abnormality in test batteries with multiple measures. Neuropsychology, 10, 120–124.CrossRefGoogle Scholar
Intitute of Medicine. (2012). The public health dimensions of the epilepsies - Institute of Medicine.Google Scholar
Jalava, M., Sillanpää, M., Camfield, C., & Camfield, P. (1997). Social adjustment and competence 35 years after onset of childhood epilepsy: A prospective controlled study. Epilepsia, 38(6), 708–715.CrossRefGoogle ScholarPubMed
Kaaden, S., & Helmstaedter, C. (2009). Age at onset of epilepsy as a determinant of intellectual impairment in temporal lobe epilepsy. Epilepsy & Behavior, 15(2), 213–217.CrossRefGoogle ScholarPubMed
Koponen, A., Seppälä, U., Eriksson, K., Nieminen, P., Uutela, A., Sillanpää, M., & Kälviäinen, R. (2007). Social functioning and psychological well-being of 347 young adults with epilepsy only--population-based, controlled study from Finland. Epilepsia, 48(5), 907–912.CrossRefGoogle Scholar
Laine, M., Koivuselkä-Sallinen, P., Hänninen, R., & Niemi, J. (1997). Bostonin nimentätestin suomenkielinen versio [Finnish version of the Boston Naming Test]. Helsinki: Psykologien kustannus.Google Scholar
Lezak, M.D., Howieson, D.B., Bigler, E.D., & Tranel, D. (2012). Neuropsychological assessment. Oxford University Press, USA.Google Scholar
Lin, J.J., Mula, M., & Hermann, B.P. (2012). Uncovering the neurobehavioural comorbidities of epilepsy over the lifespan. Lancet, 380(9848), 1180–1192.CrossRefGoogle ScholarPubMed
Loring, D.W., Strauss, E., Hermann, B.P., Barr, W.B., Perrine, K., Trenerry, M.R., & Bowden, S.C. (2008). Differential neuropsychological test sensitivity to left temporal lobe epilepsy. Journal of the International Neuropsychological Society, 14(3), 394–400.CrossRefGoogle ScholarPubMed
MacAllister, W.S., & Schaffer, S.G. (2007). Neuropsychological deficits in childhood epilepsy syndromes. Neuropsychology Review, 17(4), 427–444.CrossRefGoogle ScholarPubMed
Oyegbile, T.O., Dow, C., Jones, J., Bell, B., Rutecki, P., Sheth, R., & Hermann, B.P. (2004). The nature and course of neuropsychological morbidity in chronic temporal lobe epilepsy. Neurology, 62(10), 1736–1742.CrossRefGoogle ScholarPubMed
Poutiainen, E., Kalska, H., & Laasonen, M. (2010). Trail making-testi [Finnish manual for the Trail Making Test]. Helsinki: Hogrefe Psykologien kustannus.Google Scholar
Pulliainen, V., Kuikka, P., & Jokelainen, M. (2000). Motor and cognitive functions in newly diagnosed adult seizure patients before antiepileptic medication. Acta Neurologica Scandinavica, 101(2), 73–78.CrossRefGoogle ScholarPubMed
Rudzinski, L.A., & Meador, K.J. (2013). Epilepsy and neuropsychological comorbidities. Continuum (Minneapolis, Minn.), 19(3 Epilepsy), 682–696.Google ScholarPubMed
Schmidt, M. (1996). Rey Auditory and Verbal Learning Test: A handbook. Los Angeles, CA: Western Psychological Services.Google Scholar
Schoenfeld, J., Seidenberg, M., Woodard, A., Hecox, K., Inglese, C., Mack, K., & & Hermann, B. (1999). Neuropsychological and behavioral status of children with complex partial seizures. Developmental Medicine and Child Neurology, 41(11), 724–731.CrossRefGoogle ScholarPubMed
Seidenberg, M., Pulsipher, D.T., & Hermann, B. (2007). Cognitive progression in epilepsy. Neuropsychology Review, 17(4), 445–454.CrossRefGoogle ScholarPubMed
Sillanpää, M., Anttinen, A., Rinne, J.O., Joutsa, J., Sonninen, P., Erkinjuntti, M., & Shinnar, S. (2015). Childhood-onset epilepsy five decades later. A prospective population-based cohort study. Epilepsia, 56(11), 1774–1783.CrossRefGoogle Scholar
Sillanpää, M., Jalava, M., Kaleva, O., & Shinnar, S. (1998). Long-term prognosis of seizures with onset in childhood. The New England Journal of Medicine, 338(24), 1715–1722.CrossRefGoogle ScholarPubMed
Sillanpää, M. (1973). Medico-social prognosis of children with epilepsy. Epidemiological study and analysis of 245 patients. Acta Paediatrica Scandinavica. Supplement, 237, 3–104.Google ScholarPubMed
Sillanpää, M., Haataja, L., & Shinnar, S. (2004). Perceived impact of childhood-onset epilepsy on quality of life as an adult. Epilepsia, 45(8), 971–977.CrossRefGoogle ScholarPubMed
Sillanpää, M., & Schmidt, D. (2010). Long-term employment of adults with childhood-onset epilepsy: A prospective population-based study. Epilepsia, 51(6), 1053–1060.CrossRefGoogle ScholarPubMed
Sogawa, Y., Masur, D., O’Dell, C., Moshe, S. L., & Shinnar, S. (2010). Cognitive outcomes in children who present with a first unprovoked seizure. Epilepsia, 51(12), 2432–2439.CrossRefGoogle ScholarPubMed
Speechley, K.N., Ferro, M.A., Camfield, C.S., Huang, W., Levin, S.D., Smith, M.L., & Zou, G. (2012). Quality of life in children with new-onset epilepsy: A 2-year prospective cohort study. Neurology, 79(15), 1548–1555.CrossRefGoogle ScholarPubMed
SPSS Inc. (2009). PASW Statistics for Windows 18.Google Scholar
Vingerhoets, G. (2006). Cognitive effects of seizures. Seizure, 15(4), 221–226.CrossRefGoogle ScholarPubMed
Wechsler, D. (1992). WAIS-R käsikirja [Manual of the Finnish version of WAIS-R]. Helsinki: Psykologien kustannus.Google Scholar
Wechsler, D. (1996). WMS-R käsikirja [Manual of the Finnish version of WMS-R]. Helsinki: Psykologien kustannus.Google Scholar