Individualised prediction of drug resistance and seizure recurrence after medication withdrawal in people with juvenile myoclonic epilepsy: A systematic review and individual participant data meta-analysis

Remi Stevelink^{1

2}, Dania Al-Toma¹, Floor E Jansen¹, Herm J Lamberink¹, Ali A Asadi-Pooya^{3

4}, Mohsen Farazdaghi³, Gonçalo Cação⁵, Sita Jayalakshmi⁶, Anuja Patil⁶, Çiğdem Özkara⁷, Şenay Aydın⁸, Joanna Gesche^{9

10}, Christoph P Beier^{9

10}, Linda J Stephen¹¹, Martin J Brodie¹¹, Gopeekrishnan Unnithan¹², Ashalatha Radhakrishnan¹², Julia Höfler¹³, Eugen Trinka^{13

14

15}, Roland Krause¹⁶; EpiPGX Consortium; Emanuele Cerulli Irelli¹⁷, Carlo Di Bonaventura¹⁷, Jerzy P Szaflarski¹⁸, Laura E Hernández-Vanegas¹⁹, Monica L Moya-Alfaro¹⁹, Yingying Zhang²⁰, Dong Zhou²⁰, Nicola Pietrafusa²¹, Nicola Specchio²¹, Giorgi Japaridze²², Sándor Beniczky^{23

24}, Mubeen Janmohamed²⁵, Patrick Kwan^{25

26}, Marte Syvertsen²⁷, Kaja K Selmer²⁸, Bernd J Vorderwülbecke²⁹, Martin Holtkamp²⁹, Lakshminarayanapuram G Viswanathan³⁰, Sanjib Sinha³⁰, Betül Baykan³¹, Ebru Altindag³², Felix von Podewils³³, Juliane Schulz³³, Udaya Seneviratne^{34

35}, Alejandro Viloria-Alebesque^{36

37}, Ioannis Karakis³⁸, Wendyl J D'Souza³⁴, Josemir W Sander^{20

39

40}, Bobby P C Koeleman², Willem M Otte¹, Kees P J Braun¹

Affiliations

¹ Department of Child Neurology, UMC Utrecht Brain Center, University Medical Center Utrecht, European Reference Network EpiCARE, Heidelberglaan 100, Utrecht, 3584 CX, Netherlands.
² Department of Genetics, Center for Molecular Medicine, University Medical Center Utrecht, European Reference Network EpiCARE, Heidelberglaan 100, Utrecht, 3584 CX, Netherlands.
³ Epilepsy Research Center, Shiraz University of Medical Sciences, Zand, Shiraz, Iran.
⁴ Department of Neurology, Thomas Jefferson University, 909 Walnut Street, Philadelphia, PA, 19107, USA.
⁵ Department of Neurology, Unidade Local de Saude do Alto Minho, Estrada de Santa Luzia, Viana do Castelo, 4904-858, Portugal.
⁶ Department of Neurology, Krishna Institute of Medical Sciences, Minister Road, Secunderabad, 500003, India.
⁷ Department of Neurology, Cerrahpasa Faculty of Medicine, Istanbul University-Cerrahpaşa, Kocamustafapaşa caddesi, Istanbul, 34098, Turkey.
⁸ Department of Neurology, Yedikule Chest Diseases and Chest Surgery Training and Research Hospital, University of Health Sciences, Belgrat Kapı yolu, Istanbul, 34020, Turkey.
⁹ Department of Neurology, Odense University Hospital, J.B. Winsløws Vej 4, Odense, 5000, Denmark.
¹⁰ Department of Clinical Research, University of Southern Denmark, J.B. Winsløws Vej 4, Odense, 5000, Denmark.
¹¹ Epilepsy Unit, University of Glasgow, University Avenue, Glasgow, G12 8QQ, UK.
¹² Department of Neurology, R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Chalakkuzhi, Medical College Road, Trivandrum, 695011, India.
¹³ Department of Neurology and Neuroscience Institute, Christian Doppler Medical Centre, Paracelsus Medical University and Centre for Cognitive Neuroscience, European Reference Network EpiCARE, Ignaz-Harrer Straße 79, Salzburg, 5020, Austria.
¹⁴ Karl Landsteiner Institute for Neurorehabilitation and Space Neurology, Hellbrunner Straße 34, Salzburg, 3100, Austria.
¹⁵ Department of Public Health, University for Health Sciences, Medical Informatics and Technology, Eduard-Wallnöfer-Zentrum 1, Hall in Tirol, 6060, Austria.
¹⁶ Bioinformatics Core Facility, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, 6 Ave du Swing, Belvaux, 4367, Luxembourg.
¹⁷ Department of Human Neurosciences, Epilepsy Unit, Sapienza, University of Rome, Viale dell'Università 30, Rome, 00185, Italy.
¹⁸ Departments of Neurology, Neurosurgery, and Neurobiology, UAB Epilepsy Center, University of Alabama at Birmingham Heersink School of Medicine, 1670 University Blvd, Birmingham, AL, 35294, USA.
¹⁹ Department of Clinical Research, Epilepsy Clinic, National Institute of Neurology and Neurosurgery, Insurgentes Sur 3877, Mexico, 14269, Mexico.
²⁰ Department of Neurology, West China Hospital of Sichuan University, 37 Guoxue Road, Chengdu, 610000, China.
²¹ Department of Neuroscience, Division of Neurology, Bambino Gesù Children's Hospital, IRCCS, Piazza Sant'Onofrio, 4, Rome, 00165, Italy.
²² Department of Clinical Neurophysiology, Institute of Neurology and Neuropsychology, 83/11 Vazha-Pshavela Ave., Tbilisi, 186, Georgia.
²³ Department of Clinical Neurophysiology, Danish Epilepsy Centre, Filadelfia, Visby Allé 5, Dianalund, 4293, Denmark.
²⁴ Department of Clinical Neurophysiology, Aarhus University Hospital and Aarhus University, Palle Juul-Jensens Blvd. 99, Aarhus, 8200, Denmark.
²⁵ Department of Neurosciences, Central Clinical School, Monash University, 99 Commercial Road, Melbourne, Victoria, 3004, Australia.
²⁶ Departments of Medicine and Neurology, Royal Melbourne Hospital, University of Melbourne, Grattan Street, Parkville, Victoria, Australia.
²⁷ Department of Neurology, Vestre Viken Hospital Trust, Dronninggata 28, Drammen, 3004, Norway.
²⁸ National Centre for Epilepsy & Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, G. F. Henriksens vei 29, Sandvika, 1337, Norway.
²⁹ Department of Neurology, Epilepsy-Center Berlin-Brandenburg, Charité - Universitätsmedizin Berlin, Charitéplatz 1, Berlin, 10117, Germany.
³⁰ Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Hosur Road, Bangalore, 560029, India.
³¹ Department of Neurology and Clinical Neurophysiology, Istanbul Faculty of Medicine, Istanbul University, Millet Cad, Istanbul, 34390, Turkey.
³² Department of Neurology, Istanbul Florence Nightingale Hospital, Abide-i Hürriyet Cad, Istanbul, 34381, Turkey.
³³ Department of Neurology, Epilepsy Center, University Medicine Greifswald, Sauerbruchstraße, Greifswald, 17489, Germany.
³⁴ Department of Medicine, St Vincent's Hospital Melbourne, The University of Melbourne, 55 Victoria Parade, Melbourne, Victoria, 3065, Australia.
³⁵ Department of Medicine, The School of Clinical Sciences at Monash Health, Monash University, Clayton Road, Melbourne, Victoria, 3168, Australia.
³⁶ Department of Neurology, Hospital General de la Defensa, Vía Ibérica 1, Zaragoza, 50009, Spain.
³⁷ Instituto de Investigación Sanitaria (IIS) Aragón, Avda. San Juan Bosco 13, Zaragoza, 50009, Spain.
³⁸ Department of Neurology, Emory University School of Medicine, 49 Jesse Hill Jr. Drive SE, Office 335, Atlanta, GA, 30303, USA.
³⁹ Stichting Epilepsie Instellingen Nederland (SEIN), Achterweg 7, Heemstede, Netherlands.
⁴⁰ UCL Queen Square Institute of Neurology, Queen Square, London, WC1N 3BG, UK.

PMID: 36467455
PMCID: PMC9716332
DOI: 10.1016/j.eclinm.2022.101732

Individualised prediction of drug resistance and seizure recurrence after medication withdrawal in people with juvenile myoclonic epilepsy: A systematic review and individual participant data meta-analysis

Remi Stevelink et al. EClinicalMedicine. 2022.

. 2022 Nov 11:53:101732.

doi: 10.1016/j.eclinm.2022.101732. eCollection 2022 Nov.

Authors

Affiliations

¹ Department of Child Neurology, UMC Utrecht Brain Center, University Medical Center Utrecht, European Reference Network EpiCARE, Heidelberglaan 100, Utrecht, 3584 CX, Netherlands.
² Department of Genetics, Center for Molecular Medicine, University Medical Center Utrecht, European Reference Network EpiCARE, Heidelberglaan 100, Utrecht, 3584 CX, Netherlands.
³ Epilepsy Research Center, Shiraz University of Medical Sciences, Zand, Shiraz, Iran.
⁴ Department of Neurology, Thomas Jefferson University, 909 Walnut Street, Philadelphia, PA, 19107, USA.
⁵ Department of Neurology, Unidade Local de Saude do Alto Minho, Estrada de Santa Luzia, Viana do Castelo, 4904-858, Portugal.
⁶ Department of Neurology, Krishna Institute of Medical Sciences, Minister Road, Secunderabad, 500003, India.
⁷ Department of Neurology, Cerrahpasa Faculty of Medicine, Istanbul University-Cerrahpaşa, Kocamustafapaşa caddesi, Istanbul, 34098, Turkey.
⁸ Department of Neurology, Yedikule Chest Diseases and Chest Surgery Training and Research Hospital, University of Health Sciences, Belgrat Kapı yolu, Istanbul, 34020, Turkey.
⁹ Department of Neurology, Odense University Hospital, J.B. Winsløws Vej 4, Odense, 5000, Denmark.
¹⁰ Department of Clinical Research, University of Southern Denmark, J.B. Winsløws Vej 4, Odense, 5000, Denmark.
¹¹ Epilepsy Unit, University of Glasgow, University Avenue, Glasgow, G12 8QQ, UK.
¹² Department of Neurology, R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Chalakkuzhi, Medical College Road, Trivandrum, 695011, India.
¹³ Department of Neurology and Neuroscience Institute, Christian Doppler Medical Centre, Paracelsus Medical University and Centre for Cognitive Neuroscience, European Reference Network EpiCARE, Ignaz-Harrer Straße 79, Salzburg, 5020, Austria.
¹⁴ Karl Landsteiner Institute for Neurorehabilitation and Space Neurology, Hellbrunner Straße 34, Salzburg, 3100, Austria.
¹⁵ Department of Public Health, University for Health Sciences, Medical Informatics and Technology, Eduard-Wallnöfer-Zentrum 1, Hall in Tirol, 6060, Austria.
¹⁶ Bioinformatics Core Facility, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, 6 Ave du Swing, Belvaux, 4367, Luxembourg.
¹⁷ Department of Human Neurosciences, Epilepsy Unit, Sapienza, University of Rome, Viale dell'Università 30, Rome, 00185, Italy.
¹⁸ Departments of Neurology, Neurosurgery, and Neurobiology, UAB Epilepsy Center, University of Alabama at Birmingham Heersink School of Medicine, 1670 University Blvd, Birmingham, AL, 35294, USA.
¹⁹ Department of Clinical Research, Epilepsy Clinic, National Institute of Neurology and Neurosurgery, Insurgentes Sur 3877, Mexico, 14269, Mexico.
²⁰ Department of Neurology, West China Hospital of Sichuan University, 37 Guoxue Road, Chengdu, 610000, China.
²¹ Department of Neuroscience, Division of Neurology, Bambino Gesù Children's Hospital, IRCCS, Piazza Sant'Onofrio, 4, Rome, 00165, Italy.
²² Department of Clinical Neurophysiology, Institute of Neurology and Neuropsychology, 83/11 Vazha-Pshavela Ave., Tbilisi, 186, Georgia.
²³ Department of Clinical Neurophysiology, Danish Epilepsy Centre, Filadelfia, Visby Allé 5, Dianalund, 4293, Denmark.
²⁴ Department of Clinical Neurophysiology, Aarhus University Hospital and Aarhus University, Palle Juul-Jensens Blvd. 99, Aarhus, 8200, Denmark.
²⁵ Department of Neurosciences, Central Clinical School, Monash University, 99 Commercial Road, Melbourne, Victoria, 3004, Australia.
²⁶ Departments of Medicine and Neurology, Royal Melbourne Hospital, University of Melbourne, Grattan Street, Parkville, Victoria, Australia.
²⁷ Department of Neurology, Vestre Viken Hospital Trust, Dronninggata 28, Drammen, 3004, Norway.
²⁸ National Centre for Epilepsy & Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, G. F. Henriksens vei 29, Sandvika, 1337, Norway.
²⁹ Department of Neurology, Epilepsy-Center Berlin-Brandenburg, Charité - Universitätsmedizin Berlin, Charitéplatz 1, Berlin, 10117, Germany.
³⁰ Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Hosur Road, Bangalore, 560029, India.
³¹ Department of Neurology and Clinical Neurophysiology, Istanbul Faculty of Medicine, Istanbul University, Millet Cad, Istanbul, 34390, Turkey.
³² Department of Neurology, Istanbul Florence Nightingale Hospital, Abide-i Hürriyet Cad, Istanbul, 34381, Turkey.
³³ Department of Neurology, Epilepsy Center, University Medicine Greifswald, Sauerbruchstraße, Greifswald, 17489, Germany.
³⁴ Department of Medicine, St Vincent's Hospital Melbourne, The University of Melbourne, 55 Victoria Parade, Melbourne, Victoria, 3065, Australia.
³⁵ Department of Medicine, The School of Clinical Sciences at Monash Health, Monash University, Clayton Road, Melbourne, Victoria, 3168, Australia.
³⁶ Department of Neurology, Hospital General de la Defensa, Vía Ibérica 1, Zaragoza, 50009, Spain.
³⁷ Instituto de Investigación Sanitaria (IIS) Aragón, Avda. San Juan Bosco 13, Zaragoza, 50009, Spain.
³⁸ Department of Neurology, Emory University School of Medicine, 49 Jesse Hill Jr. Drive SE, Office 335, Atlanta, GA, 30303, USA.
³⁹ Stichting Epilepsie Instellingen Nederland (SEIN), Achterweg 7, Heemstede, Netherlands.
⁴⁰ UCL Queen Square Institute of Neurology, Queen Square, London, WC1N 3BG, UK.

PMID: 36467455
PMCID: PMC9716332
DOI: 10.1016/j.eclinm.2022.101732

Abstract

Background: A third of people with juvenile myoclonic epilepsy (JME) are drug-resistant. Three-quarters have a seizure relapse when attempting to withdraw anti-seizure medication (ASM) after achieving seizure-freedom. It is currently impossible to predict who is likely to become drug-resistant and safely withdraw treatment. We aimed to identify predictors of drug resistance and seizure recurrence to allow for individualised prediction of treatment outcomes in people with JME.

Methods: We performed an individual participant data (IPD) meta-analysis based on a systematic search in EMBASE and PubMed - last updated on March 11, 2021 - including prospective and retrospective observational studies reporting on treatment outcomes of people diagnosed with JME and available seizure outcome data after a minimum one-year follow-up. We invited authors to share standardised IPD to identify predictors of drug resistance using multivariable logistic regression. We excluded pseudo-resistant individuals. A subset who attempted to withdraw ASM was included in a multivariable proportional hazards analysis on seizure recurrence after ASM withdrawal. The study was registered at the Open Science Framework (OSF; https://osf.io/b9zjc/).

Findings: Our search yielded 1641 articles; 53 were eligible, of which the authors of 24 studies agreed to collaborate by sharing IPD. Using data from 2518 people with JME, we found nine independent predictors of drug resistance: three seizure types, psychiatric comorbidities, catamenial epilepsy, epileptiform focality, ethnicity, history of CAE, family history of epilepsy, status epilepticus, and febrile seizures. Internal-external cross-validation of our multivariable model showed an area under the receiver operating characteristic curve of 0·70 (95%CI 0·68-0·72). Recurrence of seizures after ASM withdrawal (n = 368) was predicted by an earlier age at the start of withdrawal, shorter seizure-free interval and more currently used ASMs, resulting in an average internal-external cross-validation concordance-statistic of 0·70 (95%CI 0·68-0·73).

Interpretation: We were able to predict and validate clinically relevant personalised treatment outcomes for people with JME. Individualised predictions are accessible as nomograms and web-based tools.

Funding: MING fonds.

Keywords: Drug resistance; Individual participant data; JME; Juvenile myoclonic epilepsy; Medication withdrawal; Meta-analysis; Multivariable prediction; Prediction model; Refractory epilepsy; Remission; Seizure recurrence.

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Conflict of interest statement

AAA received a grant from the 10.13039/501100012155National Institute for Medical Research Development, royalties for a book publication from 10.13039/501100007723Oxford University Press, and speaker fees from Cobel Daruo, Tekaje, and Raymand Rad. CPB received research grants and honoraria from 10.13039/100011110UCB and 10.13039/501100003769Eisai, support for attending meetings by UCB, and served in the advisory board of Arvelle. CDB received consulting fees and honoraria from 10.13039/100014114GW Pharmaceuticals, 10.13039/100015661UCB Pharma, 10.13039/501100003769Eisai, 10.13039/501100006546Angelini Pharma and Bial. JPS received grants from the 10.13039/100000002National Institutes of Health, 10.13039/100000005Department of Defense, and the 10.13039/100000001National Science Foundation; and consulting fees from 10.13039/100015661UCB Pharma, AdCel Biopharma, LLC, iFovea, SK Life Sciences, and 10.13039/100013410LivaNova; and has stock options for iFovea and AdCel Biopharma. LEH-V participates in the Young Epilepsy Society, received speaker honorario from Armstrong, and was supported by Abbott pharmaceuticals to attend the Mexican Congress of Neurology. NP received honoraria from Zogenix and Ethos for Angelini Pharma. NS received honoraria from Biomarin, Livanova, GW Pharma, Zogenix and Marinus; and support to attend meetings from Livanova, GW Pharma and Zogenix; and participated on a data safety monitoring board for Marinus. SB received speaker fees from Eisai. PK received lecture honorarium from UCB Pharma and Eisai, consulting fees from 10.13039/501100003769Eisai and 10.13039/100013410LivaNova and his institution received research grants from 10.13039/100015661UCB Pharma and 10.13039/501100003769Eisai. MS received speaker honoraria from UCB Pharma and Eisai. KKS received research grants from the 10.13039/501100005416Norwegian Research Council, the DAMFoundation and the Norwegian National Advisory Unit on Rare diseases; and a networking grant from the 10.13039/501100004785NordForsk Foundation; and she acted as a paid PhD defense opponent at the University of Bergen, and attended a meeting for Nordic clinicians organised by Eisai. BJV received grants from the 10.13039/501100007870German Society for Epileptology and the 10.13039/501100001659Deutsche Forschungsgemeinschaft; and honoraria from University Medical Center Schleswig–Holstein and Cornelsen Verlag. MH received consulting fees and honoraria from Arvelle, Bial, Desitin, Eisai, GW Pharmaceuticals, UCB Pharma, and Zogenix. FvP has received speaker honoraria from Bial, Eisai, GW Pharmaceutical companies, Angelinipharma, Zogenix and UCB Pharma; and scientific advisory board honoraria from GW Pharmaceutical companies, UCB Pharma, and Angelinipharma. WD's salary is part-funded by The University of Melbourne; he has received travel, investigator-initiated, scientific advisory board and speaker honoraria from UCB Pharma Australia and Global; investigator-initiated, scientific advisory board, travel and speaker honoraria from Eisai Australia and Global; advisory board honoraria from Liva Nova and Tilray; educational grants from Novartis Pharmaceuticals, 10.13039/100014476Pfizer Pharmaceuticals and Sanofi-Synthelabo; educational; travel and fellowship grants from GSK Neurology Australia, and honoraria from SciGen Pharmaceuticals; and he has an equity interest in the device company EpiMinder. CPB received honaries and research support from EISAI, UCB and Arvelle. ET received speaker's honoraria from Arvelle, Abbott, Angelini Pharma, UCB, Biogen, Gerot-Lannacher, Bial, Eisai, Epilog, Takeda, Newbridge, Hikma, GW Pharmaceuticals, Sunovion Pharmaceuticals Inc., LivaNova and Novartis; consultancy funds from 10.13039/501100006546Angelini Pharma, Argenix, Arvelle, Epilog, 10.13039/100011110UCB, 10.13039/100005614Biogen, Gerot-Lannach, Bial, 10.13039/501100003769Eisai, 10.13039/100007723Takeda, Newbridge, 10.13039/100014114GW Pharmaceuticals, 10.13039/100009655Sunovion Pharmaceuticals Inc., Marinus, and 10.13039/100004336Novartis; directorship funds from Neuroconsult GmbH. ET's Institution received grants from 10.13039/100005614Biogen, Red Bull, 10.13039/100004334Merck, 10.13039/100011110UCB, 10.13039/501100000780European Union, FWF Österreichischer Fond zur Wissenschaftsförderung, and 10.13039/501100007148Bundesministerium für Wissenschaft und Forschung. JWS reports personal fees from Arvelle, personal fees from 10.13039/100011110UCB, grants from UCB, grants from 10.13039/100003997NEF, grants from UCB, personal fees from 10.13039/100012739Zogenix, grants from GW Phama, outside the submitted work; and his current position is endowed by the Epilepsy Society, he is a member of the Editorial Board of the Lancet Neurology, and receives research support from the Marvin Weil Epilepsy Research Fund. All other authors declare no potential competing interests. None of the above mentioned declarations represent a conflict of interest directly related to the present publication.

Figures

**Fig. 1**
Flowchart of search strategy and study selection.s

**Fig. 2**
**(A)** Nomogram for prediction of drug-resistant JME. For example, a Caucasian (18 points) girl with a history of febrile seizures (9), who never had a status epilepticus, who has a psychiatric comorbidity (12.5), no family history of epilepsy (0), three seizure types (19.5), catamenial epilepsy (13), focal epileptiform activity on EEG (17), no history of childhood absence epilepsy (CAE; 0), has a total 89 points, corresponding to a 90% risk of drug resistance. **(B)** Calibration plot comparing observed and predicted probabilities, which should ideally follow the diagonal line.

**Fig. 3**
**Survival curve for seizure-freedom after initiation of ASM withdrawal.** Freedom of any seizure after withdrawal (blue) and freedom of generalised tonic-clonic seizures (GTCS; red) after withdrawal are displayed, with the 95% confidence interval in shaded colours. The X-axis represents the years after start of withdrawal. The number of individuals at risk is displayed below risk for each time point.

**Fig. 4**
**(A)** Nomogram for predicting recurrence of any seizure after ASM withdrawal in people with JME. For example, someone with JME who is 44 years old at initiating withdrawal (6 points), who has been seizure-free for the last four years (6 points) and is currently using 1 ASM (0 points) has a total score of 12, which corresponds to a 37% chance of recurrence in 2 years and a 48% chance of recurrence at five years. **(B)** Calibration plot comparing observed and predicted probabilities, which should ideally follow the diagonal line.

See this image and copyright information in PMC

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Individualised prediction of drug resistance and seizure recurrence after medication withdrawal in people with juvenile myoclonic epilepsy: A systematic review and individual participant data meta-analysis

Affiliations

Individualised prediction of drug resistance and seizure recurrence after medication withdrawal in people with juvenile myoclonic epilepsy: A systematic review and individual participant data meta-analysis

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Grants and funding

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