Polygenic burden in focal and generalized epilepsies

doi:10.1093/brain/awz292

Comparative Study

. 2019 Nov 1;142(11):3473-3481.

doi: 10.1093/brain/awz292.

Polygenic burden in focal and generalized epilepsies

Costin Leu^{1

2

3}, Remi Stevelink⁴, Alexander W Smith², Slavina B Goleva^{5

6}, Masahiro Kanai^{2

7

8

9

10}, Lisa Ferguson^{11

12

13}, Ciaran Campbell^{14

15}, Yoichiro Kamatani^{10

16}, Yukinori Okada^{10

17

18}, Sanjay M Sisodiya^{3

19}, Gianpiero L Cavalleri^{14

15}, Bobby P C Koeleman⁴, Holger Lerche²⁰, Lara Jehi^{11

13}, Lea K Davis^{5

6}, Imad M Najm^{11

13}, Aarno Palotie^{2

21}, Mark J Daly^{2

7

21}, Robyn M Busch^{11

12

13}; Epi25 Consortium; Dennis Lal^{1

2

11

22}

Collaborators, Affiliations

Collaborators

Epi25 Consortium:
Liam Abbott, Zaid Afawi, Danielle Andrade, Grazia Annesi, Mutluay Arslan, Pauls Auce, Pia Auvinen, Andreas van Baalen, Melanie Bahlo, Simona Balestrini, Nina Barišic, Jürgen Bauer, Larry Baum, Betül Baykan, Nerses Bebek, Felicitas Becker, Susannah Bellows, Caitlin Bennett, Samuel Berkovic, Claudia Bianchini, Francesca Bisulli, Ilan Blatt, Ingo Borggräfe, Vera Braatz, Knut Brockmann, Russell Buono, Rosemary Burgess, Hande Caglayan, Laura Canafoglia, Christina Canavati, Barbara Castellotti, Gianpiero Cavalleri, Felecia Cerrato, Stacey Cherny, Seo-Kyung Chung, Claire Churchhouse, Valentina Ciullo, Patrick Cossette, Chris Cotsapas, Norman Delanty, Dieter Dennig, Chantal Depondt, Orrin Devinsky, Tracy Dixon-Salazar, Dennis Dlugos, Viola Doccini, Colin Doherty, Christian Elger, Colin Ellis, Hany El-Naggar, Yen-Chen Anne Feng, Thomas Ferraro, Silvana Franceschetti, Jacqueline French, Catharine Freyer, Monica Gagliardi, Sabina Gallati, Antonio Gambardella, Tommaso Gili, David Goldstein, Tiziana Granata, Jurgita Grikiniene, Renzo Guerrini, Asli Gundogdu-Eken, Namrata Gupta, Hakon Hakonarson, Garen Haryanyan, Martin Häusler, Manu Hegde, Erin Heinzen, Katherine Helbig, Ingo Helbig, Christian Hengsbach, Daniel Howrigan, Michele Iacomino, Yushi Inoue, Esther Johns, Michael Johnson, Peter De Jonghe, Reetta Kälviäinen, Sitharthan Kamalakaran, Moien Kanaan, Bulent Kara, Yesim Kesim, Pouya Khankhanian, Chontelle King, Karl Klein, Gerhard Kluger, Susanne Knake, Amos Korczyn, Rudolf Korinthenberg, Ioanna Kousiappa, Roland Krause, Heinz Krestel, Ilona Krey, Wolfram Kunz, Gerhard Kurlemann, Ruben Kuzniecky, Patrick Kwan, Angelo Labate, Dennis Lal, Petra Laššuthová, Anna-Elina Lehesjoki, Johannes Lemke, Holger Lerche, Costin Leu, Laura Licchetta, Tarja Linnankivi, Warren Lo, Daniel Lowenstein, Colin Lui, Alexandra Macdonald, Rene Madeleyn, Francesca Madia, Ana Maisch, Ruta Mameniskiene, Maria Mancardi, Lorella Manna, Carla Marini, Anthony Marson, Patrick May, Thomas Mayer, Mark McCormack, Kevin McKenna, Davide Mei, Raffaella Minardi, Kelly Mo, Martino Montomoli, Emily Mountier, Lorenzo Muccioli, Hiltrud Muhle, Karen Müller-Schlüter, Benjamin Neale, Terence O'Brien, Çigdem Özkara, Savvas Papacostas, Elena Parrini, Manuela Pendziwiat, Slavé Petrovski, William Pickrell, Tommaso Pippucci, Fabrizio Piras, Federica Piras, Annapurna Poduri, Robert Powell, Ruta Praninskiene, Michael Privitera, Annika Rademacher, Michael Rademacher, Sarah Rau, Mark Rees, Brigid Regan, Philipp Reif, Felix Rosenow, Anni Saarela, Lynette Sadleir, Tara Sadoway, Baris Salman, Vincenzo Salpietro, Ruta Samaitiene, Steven Schachter, Christoph Schankin, Ingrid Scheffer, Natascha Schneider, Herbert Schreiber, Susanne Schubert-Bast, Andreas Schulze-Bonhage, Lucie Sedlácková, Catherine Shain, Pak Sham, Beth Sheidley, Hannah Shilling, Arif Shukralla, Graeme Sills, Sanjay Sisodiya, Gianfranco Spalletta, Michael Sperling, Sarah von Spiczak, Hannah Stamberger, Bernhard Steinhoff, Ulrich Stephani, Katalin Šterbová, Randy Stewart, Carlotta Stipa, Pasquale Striano, Toshimitsu Suzuki, George Tanteles, Katherine Tashman, Paolo Tinuper, Marian Todaro, Pinar Topaloglu, Birute Tumiene, Dilsad Turkdogan, Sibel Ugur-Iseri, Algirdas Utkus, Maria Stella Vari, Annalisa Vetro, Markéta Vlcková, Yvonne Weber, Dorien Weckhuysen, Sarah Weckhuysen, Stefan Wolking, Kazuhiro Yamakawa, Zuhal Yapici, Uluc Yis, Emrah Yücesan, Sara Zagaglia, Federico Zara, Gábor Zsurka

Affiliations

¹ Genomic Medicine Institute, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA.
² Stanley Center for Psychiatric Research, Broad Institute of Harvard and M.I.T, Cambridge, MA, USA.
³ Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, Queen Square, London, UK.
⁴ Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands.
⁵ Division of Genetic Medicine, Department of Medicine, Vanderbilt University, Nashville, TN, USA.
⁶ Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN, USA.
⁷ Analytic and Translational Genetics Unit, Massachusetts General Hospital, Boston, MA, USA.
⁸ Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁹ Department of Biomedical Informatics, Harvard Medical School, Boston, MA, USA.
¹⁰ Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
¹¹ Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹² Department of Psychiatry and Psychology, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹³ Department of Neurology, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹⁴ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin 2, Ireland.
¹⁵ The FutureNeuro Research Centre, Dublin 2, Ireland.
¹⁶ Kyoto-McGill International Collaborative School in Genomic Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
¹⁷ Department of Statistical Genetics, Osaka University Graduate School of Medicine, Suita, Japan.
¹⁸ Laboratory of Statistical Immunology, Immunology Frontier Research Center (WPI-IFReC), Osaka University, Suita, Japan.
¹⁹ Chalfont Centre for Epilepsy, Chalfont-St-Peter, Buckinghamshire, UK.
²⁰ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²¹ Institute of Molecular Medicine Finland (FIMM), HiLIFE, University of Helsinki, Helsinki, Finland.
²² Cologne Center for Genomics (CCG), University of Cologne, Cologne, Germany.

PMID: 31608925
PMCID: PMC6821205
DOI: 10.1093/brain/awz292

Comparative Study

Polygenic burden in focal and generalized epilepsies

Costin Leu et al. Brain. 2019.

. 2019 Nov 1;142(11):3473-3481.

doi: 10.1093/brain/awz292.

Authors

Collaborators

Epi25 Consortium:
Liam Abbott, Zaid Afawi, Danielle Andrade, Grazia Annesi, Mutluay Arslan, Pauls Auce, Pia Auvinen, Andreas van Baalen, Melanie Bahlo, Simona Balestrini, Nina Barišic, Jürgen Bauer, Larry Baum, Betül Baykan, Nerses Bebek, Felicitas Becker, Susannah Bellows, Caitlin Bennett, Samuel Berkovic, Claudia Bianchini, Francesca Bisulli, Ilan Blatt, Ingo Borggräfe, Vera Braatz, Knut Brockmann, Russell Buono, Rosemary Burgess, Hande Caglayan, Laura Canafoglia, Christina Canavati, Barbara Castellotti, Gianpiero Cavalleri, Felecia Cerrato, Stacey Cherny, Seo-Kyung Chung, Claire Churchhouse, Valentina Ciullo, Patrick Cossette, Chris Cotsapas, Norman Delanty, Dieter Dennig, Chantal Depondt, Orrin Devinsky, Tracy Dixon-Salazar, Dennis Dlugos, Viola Doccini, Colin Doherty, Christian Elger, Colin Ellis, Hany El-Naggar, Yen-Chen Anne Feng, Thomas Ferraro, Silvana Franceschetti, Jacqueline French, Catharine Freyer, Monica Gagliardi, Sabina Gallati, Antonio Gambardella, Tommaso Gili, David Goldstein, Tiziana Granata, Jurgita Grikiniene, Renzo Guerrini, Asli Gundogdu-Eken, Namrata Gupta, Hakon Hakonarson, Garen Haryanyan, Martin Häusler, Manu Hegde, Erin Heinzen, Katherine Helbig, Ingo Helbig, Christian Hengsbach, Daniel Howrigan, Michele Iacomino, Yushi Inoue, Esther Johns, Michael Johnson, Peter De Jonghe, Reetta Kälviäinen, Sitharthan Kamalakaran, Moien Kanaan, Bulent Kara, Yesim Kesim, Pouya Khankhanian, Chontelle King, Karl Klein, Gerhard Kluger, Susanne Knake, Amos Korczyn, Rudolf Korinthenberg, Ioanna Kousiappa, Roland Krause, Heinz Krestel, Ilona Krey, Wolfram Kunz, Gerhard Kurlemann, Ruben Kuzniecky, Patrick Kwan, Angelo Labate, Dennis Lal, Petra Laššuthová, Anna-Elina Lehesjoki, Johannes Lemke, Holger Lerche, Costin Leu, Laura Licchetta, Tarja Linnankivi, Warren Lo, Daniel Lowenstein, Colin Lui, Alexandra Macdonald, Rene Madeleyn, Francesca Madia, Ana Maisch, Ruta Mameniskiene, Maria Mancardi, Lorella Manna, Carla Marini, Anthony Marson, Patrick May, Thomas Mayer, Mark McCormack, Kevin McKenna, Davide Mei, Raffaella Minardi, Kelly Mo, Martino Montomoli, Emily Mountier, Lorenzo Muccioli, Hiltrud Muhle, Karen Müller-Schlüter, Benjamin Neale, Terence O'Brien, Çigdem Özkara, Savvas Papacostas, Elena Parrini, Manuela Pendziwiat, Slavé Petrovski, William Pickrell, Tommaso Pippucci, Fabrizio Piras, Federica Piras, Annapurna Poduri, Robert Powell, Ruta Praninskiene, Michael Privitera, Annika Rademacher, Michael Rademacher, Sarah Rau, Mark Rees, Brigid Regan, Philipp Reif, Felix Rosenow, Anni Saarela, Lynette Sadleir, Tara Sadoway, Baris Salman, Vincenzo Salpietro, Ruta Samaitiene, Steven Schachter, Christoph Schankin, Ingrid Scheffer, Natascha Schneider, Herbert Schreiber, Susanne Schubert-Bast, Andreas Schulze-Bonhage, Lucie Sedlácková, Catherine Shain, Pak Sham, Beth Sheidley, Hannah Shilling, Arif Shukralla, Graeme Sills, Sanjay Sisodiya, Gianfranco Spalletta, Michael Sperling, Sarah von Spiczak, Hannah Stamberger, Bernhard Steinhoff, Ulrich Stephani, Katalin Šterbová, Randy Stewart, Carlotta Stipa, Pasquale Striano, Toshimitsu Suzuki, George Tanteles, Katherine Tashman, Paolo Tinuper, Marian Todaro, Pinar Topaloglu, Birute Tumiene, Dilsad Turkdogan, Sibel Ugur-Iseri, Algirdas Utkus, Maria Stella Vari, Annalisa Vetro, Markéta Vlcková, Yvonne Weber, Dorien Weckhuysen, Sarah Weckhuysen, Stefan Wolking, Kazuhiro Yamakawa, Zuhal Yapici, Uluc Yis, Emrah Yücesan, Sara Zagaglia, Federico Zara, Gábor Zsurka

Affiliations

¹ Genomic Medicine Institute, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA.
² Stanley Center for Psychiatric Research, Broad Institute of Harvard and M.I.T, Cambridge, MA, USA.
³ Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, Queen Square, London, UK.
⁴ Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands.
⁵ Division of Genetic Medicine, Department of Medicine, Vanderbilt University, Nashville, TN, USA.
⁶ Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN, USA.
⁷ Analytic and Translational Genetics Unit, Massachusetts General Hospital, Boston, MA, USA.
⁸ Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁹ Department of Biomedical Informatics, Harvard Medical School, Boston, MA, USA.
¹⁰ Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
¹¹ Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹² Department of Psychiatry and Psychology, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹³ Department of Neurology, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA.
¹⁴ Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin 2, Ireland.
¹⁵ The FutureNeuro Research Centre, Dublin 2, Ireland.
¹⁶ Kyoto-McGill International Collaborative School in Genomic Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
¹⁷ Department of Statistical Genetics, Osaka University Graduate School of Medicine, Suita, Japan.
¹⁸ Laboratory of Statistical Immunology, Immunology Frontier Research Center (WPI-IFReC), Osaka University, Suita, Japan.
¹⁹ Chalfont Centre for Epilepsy, Chalfont-St-Peter, Buckinghamshire, UK.
²⁰ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²¹ Institute of Molecular Medicine Finland (FIMM), HiLIFE, University of Helsinki, Helsinki, Finland.
²² Cologne Center for Genomics (CCG), University of Cologne, Cologne, Germany.

PMID: 31608925
PMCID: PMC6821205
DOI: 10.1093/brain/awz292

Erratum in

Corrigendum to: Polygenic burden in focal and generalized epilepsies.
[No authors listed] [No authors listed] Brain. 2020 Jul 1;143(7):e61. doi: 10.1093/brain/awaa091. Brain. 2020. PMID: 32268364 Free PMC article. No abstract available.

Abstract

Rare genetic variants can cause epilepsy, and genetic testing has been widely adopted for severe, paediatric-onset epilepsies. The phenotypic consequences of common genetic risk burden for epilepsies and their potential future clinical applications have not yet been determined. Using polygenic risk scores (PRS) from a European-ancestry genome-wide association study in generalized and focal epilepsy, we quantified common genetic burden in patients with generalized epilepsy (GE-PRS) or focal epilepsy (FE-PRS) from two independent non-Finnish European cohorts (Epi25 Consortium, n = 5705; Cleveland Clinic Epilepsy Center, n = 620; both compared to 20 435 controls). One Finnish-ancestry population isolate (Finnish-ancestry Epi25, n = 449; compared to 1559 controls), two European-ancestry biobanks (UK Biobank, n = 383 656; Vanderbilt biorepository, n = 49 494), and one Japanese-ancestry biobank (BioBank Japan, n = 168 680) were used for additional replications. Across 8386 patients with epilepsy and 622 212 population controls, we found and replicated significantly higher GE-PRS in patients with generalized epilepsy of European-ancestry compared to patients with focal epilepsy (Epi25: P = 1.64×10-15; Cleveland: P = 2.85×10-4; Finnish-ancestry Epi25: P = 1.80×10-4) or population controls (Epi25: P = 2.35×10-70; Cleveland: P = 1.43×10-7; Finnish-ancestry Epi25: P = 3.11×10-4; UK Biobank and Vanderbilt biorepository meta-analysis: P = 7.99×10-4). FE-PRS were significantly higher in patients with focal epilepsy compared to controls in the non-Finnish, non-biobank cohorts (Epi25: P = 5.74×10-19; Cleveland: P = 1.69×10-6). European ancestry-derived PRS did not predict generalized epilepsy or focal epilepsy in Japanese-ancestry individuals. Finally, we observed a significant 4.6-fold and a 4.5-fold enrichment of patients with generalized epilepsy compared to controls in the top 0.5% highest GE-PRS of the two non-Finnish European cohorts (Epi25: P = 2.60×10-15; Cleveland: P = 1.39×10-2). We conclude that common variant risk associated with epilepsy is significantly enriched in multiple cohorts of patients with epilepsy compared to controls-in particular for generalized epilepsy. As sample sizes and PRS accuracy continue to increase with further common variant discovery, PRS could complement established clinical biomarkers and augment genetic testing for patient classification, comorbidity research, and potentially targeted treatment.

Keywords: common variant risk; epilepsy; genetic generalized epilepsy; genetics.

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Figures

**Figure 1**
**Study design.** (1) PRSs for the two main classes of epilepsy (generalized and focal) were derived from the largest GWAS in epilepsy to date (International League Against Epilepsy Consortium on Complex Epilepsies, 2018). (2) PRS were calculated in patients with generalized or focal epilepsy and in population controls and (3) tested in their ability to identify significant differences of common variant burden among groups. (4) The UK and Vanderbilt biobanks were available to test the behaviour of the PRSs in individuals ascertained by ICD-10 codes for epilepsy, while the Biobank Japan was available to test the performance in a non-European population. SNP = single nucleotide polymorphism.

**Figure 2**
**Genome-wide polygenic risk for generalized epilepsy or focal epilepsy in the exploration and replication cohorts.** Shown are the means of the standardized GE-, FE-, and type 2 diabetes-PRS with 95% confidence intervals for the European-ancestry population controls (highlighted in blue; *n =* 20 435), the European-ancestry generalized epilepsy and focal epilepsy Epi25 exploration cohorts (highlighted in green; GE-Epi25-EUR, *n =* 2256; FE-Epi25-EUR, n = 3449), and the European-ancestry generalized epilepsy and focal epilepsy Cleveland Clinic replication cohorts (highlighted in red; GE-Cleveland-EUR, *n =* 85; FE-Cleveland-EUR, *n =* 535). The P-values for the differences between cases and population controls are given as numbers. The threshold for statistical significance after Bonferroni correction was set to α = 1.67 × 10⁻² (three tests per cohort).

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Comment in

The first step towards personalized risk prediction for common epilepsies.
Hansen TF, Møller RS. Hansen TF, et al. Brain. 2019 Nov 1;142(11):3316-3318. doi: 10.1093/brain/awz318. Brain. 2019. PMID: 31665751 No abstract available.

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References

1. Banerjee PN, Filippi D, Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res 2009; 85: 31–45. - PMC - PubMed
1. Bell GS, Neligan A, Giavasi C, Keezer MR, Novy J, Peacock JL, et al. Outcome of seizures in the general population after 25 years: a prospective follow-up, observational cohort study. J Neurol Neurosurg Psychiatry 2016; 87: 843–50. - PubMed
1. Berg AT, Shinnar S. The risk of seizure recurrence following a first unprovoked seizure: a quantitative review. Neurology 1991; 41: 965–72. - PubMed
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[1] Banerjee PN, Filippi D, Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res 2009; 85: 31–45. - PMC - PubMed

[2] Banerjee PN, Filippi D, Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res 2009; 85: 31–45. - PMC - PubMed

[3] Bell GS, Neligan A, Giavasi C, Keezer MR, Novy J, Peacock JL, et al. Outcome of seizures in the general population after 25 years: a prospective follow-up, observational cohort study. J Neurol Neurosurg Psychiatry 2016; 87: 843–50. - PubMed

[4] Bell GS, Neligan A, Giavasi C, Keezer MR, Novy J, Peacock JL, et al. Outcome of seizures in the general population after 25 years: a prospective follow-up, observational cohort study. J Neurol Neurosurg Psychiatry 2016; 87: 843–50. - PubMed

[5] Berg AT, Shinnar S. The risk of seizure recurrence following a first unprovoked seizure: a quantitative review. Neurology 1991; 41: 965–72. - PubMed

[6] Berg AT, Shinnar S. The risk of seizure recurrence following a first unprovoked seizure: a quantitative review. Neurology 1991; 41: 965–72. - PubMed

[7] Borodulin K, Tolonen H, Jousilahti P, Jula A, Juolevi A, Koskinen S, et al. Cohort profile: the National FINRISK study. Int J Epidemiol 2017. - PubMed

[8] Borodulin K, Tolonen H, Jousilahti P, Jula A, Juolevi A, Koskinen S, et al. Cohort profile: the National FINRISK study. Int J Epidemiol 2017. - PubMed

[9] Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 2015; 4: 7. - PMC - PubMed

[10] Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 2015; 4: 7. - PMC - PubMed

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Polygenic burden in focal and generalized epilepsies

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Polygenic burden in focal and generalized epilepsies

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