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Ann Clin Neurophysiol > Volume 22(2); 2020 > Article
Park, Lee, Park, and Park: Which articles have highly impacted research on genetic generalized epilepsy?

Abstract

Background

The purpose of this study was to identify the top-100 cited articles on genetic generalized epilepsy (GGE) published in journals that have made key contributions to the field of epilepsy.

Methods

We searched the Web of Science website produced by Clarivate Analytics for articles on GGE, and sorted them according to the number of citations to identify the top-100 cited articles. We then manually reviewed the contents of the top-100 cited articles, which were designated as “citation classics”.

Results

The top-100 cited articles were published in 27 journals, with the largest proportion appearing in Epilepsia (19 articles). The articles originated from institutions in 17 countries, with 31 articles from the USA. The institution associated with the largest numbers of articles in the field of GGE was the University of Melbourne, Australia (9 articles). Panayiotopoulos C. P. was the first author of three articles, and was listed most frequently in the GGE citation classics. The publication years were concentrated in the 2000s, when 56 articles were published. The most-common study topics were genetics (35 articles) and neuroimaging (17 articles).

Conclusions

This study has identified the top-100 cited articles on GGE. These citation classics represent the landmark articles on GGE, and they provide useful insights into international research leaders and the research trends in the field.

INTRODUCTION

The International League Against Epilepsy (ILAE) classification of epilepsies was updated on 2017, and it now classifies epilepsy according to seizure type, epilepsy type, and etiology.1 Generalized epilepsy refers to the seizures originating at some point within or rapidly engaging distributed networks bilaterally, the subcortical or cortical structures, or frequently both of these.1 A genetic etiology is defined when epilepsy directly results from a known or presumed genetic defect and the seizures are the core symptom of the disorder.1 The term genetic generalized epilepsy (GGE) is used when a patient has generalized seizures of genetic origin and a well-recognized and established epilepsy syndrome, and includes childhood absence epilepsy, juvenile absence epilepsy, juvenile myoclonic epilepsy, and epilepsy with tonic-clonic seizures alone.1,2 GGE has previously been termed “idiopathic generalized epilepsy,” but the ILAE recommend changing this to “genetic generalized epilepsy” due to “idiopathic” being considered too imprecise.1 Individuals with GGE account for 20% of all epilepsy cases.3 GGE occurs mostly in young people, and with a proper diagnosis and management can be controlled with medications in 80% of cases.3
The number of times that a previously published work is cited is an indicator of its recognition and impact in an area of investigation.4-6 Citation analysis is a systematic approach for identifying scientific studies that have had a high impact in a particular field. Reviewing articles that are cited frequently can provide information about the dominant areas of a discipline, as well as identify growth areas in particular fields. Furthermore, the top-cited articles are often written by recognized experts who can offer novel insight into the future directions of the discipline.4-6
Several recent studies have applied citation analysis or bibliometric analysis to various neurological fields, including stroke,7 headache disorders,8 central nervous system inflammatory demyelinating disease,9 Guillain-Barré syndrome,10 epilepsy and status epilepticus,11 and general neurology.12 However, to the best of our knowledge, no previous study has comprehensively investigated the top-cited articles in the field of GGE. The purpose of this study was to identify the top-100 cited articles (designated as “citation classics”) published in journals on GGE that have made key contributions to the field of epilepsy.

MATERIALS AND METHODS

A citation analysis is a bibliometric method that examines the frequency and patterns of citations in articles. We performed a citation analysis in the field of GGE by searching the Web of Science website (https://www.webofknowledge.com) produced by Clarivate Analytics.
In January 2020 we searched for articles published since 1950 with titles that included any of the following expressions: “genetic generalized epilepsy,” “idiopathic generalized epilepsy,” “childhood absence epilepsy,” “juvenile absence epilepsy,” “juvenile myoclonic epilepsy,” “epilepsy with generalized tonic-clonic seizures alone,” or “epilepsy with generalized tonic-clonic seizures on awakening.” The top-100 cited articles were then selected according to the number of citations, and we manually reviewed their contents. We examined various aspects of the articles, such as the number of citations, ranking, authorship, title, year of publication, publishing journal, publication type, and topic categories. The publication types were categorized into original articles, case series, and systematic reviews, and the topics were subtyped as clinical features, epidemiology, pharmacotherapy, laboratory investigations, electrophysiology, neuroimaging, genetics, neuropsychiatry, and general reviews. When the authors of an article had more than one affiliation, the department, institution, and country of origin were defined by either the first or the corresponding affiliation of the first author. Data were presented using descriptive statistics, and no tests of statistical significance were performed. This study did not need to be reviewed by an ethics committee because it performed a bibliometric analysis of existing published studies.

RESULTS

We ranked the top-100 cited articles according to the number of citations (Table 1). The most-cited and least-cited articles had been cited 580 and 76 times, respectively. Approximately two-thirds of the articles (64 articles) had been cited more than 100 times.
The top-100 cited articles were published in 27 journals (Table 2), with the largest proportion appearing in Epilepsia (19 articles), followed by Neurology (15 articles) and Brain (10 articles). The top-100 cited articles originated from institutions in 17 countries, with 31 articles from the USA, followed by the UK (14 articles), Germany (11 articles), and Australia (11 articles) (Table 3). The 100 articles comprised 40 originating from North America (the USA and Canada), 38 from Europe (the UK, Germany, France, Italy, Netherlands, Switzerland, and Sweden), 12 from Oceania (Australia and New Zealand), 8 from Asia (Saudi Arabia, China, South Korea, Israel, and Japan), and 2 from South America (Brazil).
Tables 4 and 5 list the top-ranked institutions and authors for articles published in the field of GGE, respectively. The institution associated with the largest number of articles was the University of Melbourne, Australia (nine articles), followed by the University of California in Los Angeles, USA (seven articles), and University College London, UK (six articles). Panayiotopoulos C. P. was the first author of three articles, and was listed most frequently in the GGE citation classics.
The publication years were mostly concentrated in the 2000s, when 56 articles were published. Twenty-three articles were published in the 1990s, followed by 13 articles in the 2010s, and 8 in the 1980s. The earliest recorded article was published in 1983 and the most-recent article was published in 2015.
Regarding the types of articles, 95 were original articles while 5 were systematic review articles. The subjects of the articles comprised 22 on childhood absence epilepsy, 38 on juvenile myoclonic epilepsy, and 40 on GGE as a whole. The topic subtypes of the articles comprised 35 on genetics, 17 on neuroimaging, 13 on pharmacotherapy, 13 on electrophysiology, 8 on neuropsychiatry, 5 on epidemiology, 5 on general reviews, and 4 on clinical features (Fig. 1).

DISCUSSION

This study identified and characterized the top-100 cited articles in the field of GGE. These citation classics may enable the identification of seminal advances in GGE and provide a historical perspective on the scientific progress of the field of epilepsy.
The top-ranked article had a title of “Mutant gamma-aminobutyric acid receptor subtype A (GABA)(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizure,” its first author was Wallace, it was published in Nature Genetics, and it has been cited 580 times.13 The authors found a mutation in a gene encoding a GABA(A) receptor subunit in a large family with epilepsy, and the two main phenotypes were childhood absence epilepsy and febrile seizures.13 The second-ranked article was also published in Nature Genetics, and reported that an Ala322Asp mutation in the GABRA1 gene that encodes the alpha1 subunit of GABA(A) was found in affected individuals of a large French Canadian family with juvenile myoclonic epilepsy.14 Both of these articles reported on genetic studies. The third-ranked article was a review article on childhood absence epilepsy by Crunelli V that appeared in Nature Reviews Neuroscience.
Citation analysis can identify emerging topics and the relevant trends in a particular field.5,6 The present study found that genetics was the most-common topic in the top-100 cited articles on GGE, followed by neuroimaging. Genetics and neuroimaging were the most-common topics for each decade from the 1990s to the 2010s. Since genetic epilepsy directly results from a known or presumed genetic mutation whose core symptom is seizures,1 it is not surprising that genetics was the most-common topic in the field of GGE. In addition, due to the introduction and advent of next-generation sequencing and genome-wide association studies, the development and application of high-throughput genetic testing has resulted in the discovery of hundreds of epilepsy-associated genes.15 Thus, we can assume that the number of articles on genetics will increase in the future.
The application of neuroimaging in epilepsy has also increased rapidly and evolved thanks to the substantial advancements in image-analysis techniques in recent decades.16 Early studies involving brain magnetic resonance imaging (MRI) did not reveal abnormalities in patients with GGE. However, more-recent voxel-based morphometry and structural/functional connectivity studies based on diffusion-tensor imaging and functional MRI have revealed abnormal morphologies and networks of the brain in GGE.17-20 These developments are associated with increasing numbers of related articles being published in scientific journals that could have a great impact on GGE.
The topics addressed in the citation classics varied among the decades, and we discovered some interesting trends in the topics over time. We noted that the most-cited articles on GGE were published during the 2000s. This contrasts with most bibliometric analyses on other topics demonstrating that the most-cited articles are published during the 1990s.7-11,21 Thus, we can infer that there have been considerable developments in research on GGE in recent years, which might be attributable to recent developments in research techniques such as genetics and neuroimaging in this field.
We also found that the most-cited articles were published in Epilepsia, which is the official publication of the ILAE. This is perhaps related to the epilepsy-specific journals with high impact factors being focused on GGE. Moreover, we found that about one-third of the 100 top-cited articles originated from institutions in the USA, reflecting the huge influence of the USA in health science research in general, which is probably due to both the large size of the American scientific community and its high research budget.22-25 However, a citation analysis in the field of neurology found that from half to two-thirds of the articles originated from the USA. In addition, we found that 20 articles reported on studies performed in Asia and Oceania (12 and 8 articles, respectively), which was a prominently higher ratio than in other citation analyses. We can assume that this finding is associated with the most-cited articles on GGE being published during the 2000s. Recently there have been increasing numbers of articles originating from Asia and Oceania in the field of neurology research, especially from China.26
This study is the first to perform a citation analysis of GGE. The findings could be used to identify recent advances in the field of GGE, provide a historical perspective of its scientific progress, and be used for education purposes. However, there were several inherent limitations in the research methodology. There is ongoing debate about the value of citation rates. A naïve argument is that an article of greater value will be cited more often.27 However, the number of citations could be influenced by factors other than the quality and originality of the reported research, such as the characteristics of the involved researchers, institutions, and funding agencies.21 Furthermore, analyzing the total number of citations favors older articles.28 The citation frequency of a scientific article is typically associated with a time delay of 1-2 years after its publication.29 This interval will bias evaluations of the rank and significance of recent publications. However, the use of citation rates is still widely accepted as the best method for judging the impact of the articles, with the impact factor considered indicative of the quality and rank of a given journal in its specific field of interest.30
This study has identified the top-100 cited articles on GGE. The identified citation classics represent landmark articles on GGE, and they provide useful insights into international research leaders and the research trends in the field.

Notes

Author Contributions

Conceptualization and data analysis: Kang Min Park.

Methodology: Seongho Park, Dongah Lee.

Original draft preparation: Bong Soo Park.

Conflicts of Interest

None of the authors has any conflict of interest to disclose.

Fig. 1.
Number of publications with the top-100 cited articles in the field of genetic generalized epilepsy.
acn-2020-22-2-92f1.jpg
Table 1.
The top-100 cited articles in the field of GGE
Rank Title First author Journal Year Volume First page Last page Number of citations
1 Mutant GABA(A) receptor gamma 2-subunit in childhood absence epilepsy and febrile seizures Wallace RH Nature Genetics 2001 28 49 52 580
2 Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy Cossette P Nature Genetics 2002 31 184 189 403
3 Childhood absence epilepsy: genes, channels, neurons and networks Crunelli V Nature Reviews Neuroscience 2002 3 371 382 397
4 15q13.3 microdeletions increase risk of idiopathic generalized epilepsy Helbig I Nature Genetics 2009 41 160 162 393
5 Juvenile myoclonic epilepsy of Janz Delgadoescueta AV Neurology 1984 34 285 294 310
6 Genome-wide copy number variation in epilepsy: novel susceptibility loci in idiopathic generalized and focal epilepsies Mefford HC PLOS Genetics 2010 6 1 9 308
7 Recurrent microdeletions at 15q11.2 and 16p13.11 predispose to idiopathic generalized epilepsies de Kovel CG Brain 2010 133 23 32 293
8 Juvenile myoclonic epilepsy (JME) may be linked to the BF and HLA loci on human chromosome 6 Greenberg DA American Journal of Medical Genetics 1988 31 185 192 285
9 Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy Zhang Z Brain 2011 134 2912 2928 267
10 Ethosuximide, valproic acid, and lamotrigine in childhood absence epilepsy Glauser TA New England Journal of Medicine 2010 362 790 799 262
11 fMRI activation during spike and wave discharges in idiopathic generalized epilepsy Aghakhani Y Brain 2004 127 1127 1144 260
12 Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies (retracted article. See vol 41, pg. 1043, 2009) Haug K Nature Genetics 2003 33 527 532 251
13 Coding and noncoding variation of the human calcium-channel beta(4)-subunit gene CACNB4 in patients with idiopathic generalized epilepsy and episodic ataxia Escayg A American Journal of Medical Genetics 2000 66 1531 1539 248
14 Association between genetic variation of CACNA1H and childhood absence epilepsy Chen YC Annals of Neurology 2003 54 239 243 246
15 Abnormal cerebral structure in juvenile myoclonic epilepsy demonstrated with voxel-based analysis of MRI Woermann FG Brain 1999 122 2101 2107 235
15 Epilepsy with impulsive petit mal (juvenile myoclonic epilepsy) Janz D Acta Neurologica Scandi navica 1985 72 449 459 235
17 Mutations in EFHC1 cause juvenile myoclonic epilepsy Suzuki T Nature Genetics 2004 36 842 849 229
18 Juvenile myoclonic epilepsy: a 5-year prospective study Panayiotopoulos CP Epilepsia 1994 35 285 296 225
19 Genetic mapping of a major susceptibility locus for juvenile myoclonic epilepsy on chromosome 15q Elmslie FV Human Molecular Genetics 1997 6 1329 1334 217
20 A splice-site mutation in GABRG2 associated with childhood absence epilepsy and febrile convulsions Kananura C Archives of Neurology 2002 59 1137 1141 194
21 Localization of idiopathic generalized epilepsy on chromosome 6p in families of juvenile myoclonic epilepsy patients Durner M Neurology 1991 41 1651 1655 189
22 Childhood absence epilepsy: behavioral, cognitive, and linguistic comorbidities Caplan R Epilepsia 2008 49 1838 1846 185
23 EEG-fMRI of idiopathic and secondarily generalized epilepsies Hamandi K NeuroImage 2006 31 1700 1710 179
24 Interictal mood and personality disorders in temporal lobe epilepsy and juvenile myoclonic epilepsy Perini GI Journal of Neurology Neurosurgery and Psychiatry 1996 61 601 605 170
25 Familial and sporadic 15q13.3 microdeletions in idiopathic generalized epilepsy: precedent for disorders with complex inheritance Dibbens LM Human Molecular Genetics 2009 18 3626 3631 164
26 Confirmation of linkage between juvenile myoclonic epilepsy locus and the HLA region of chromosome 6 Weissbecker KA American Journal of Medical Genetics 1991 38 32 36 160
27 Placebo-controlled study of levetiracetam in idiopathic generalized epilepsy Berkovic SF Neurology 2007 69 1751 1760 155
28 Levetiracetam for the treatment of idiopathic generalized epilepsy with myoclonic seizures Noachtar S Neurology 2008 70 607 616 153
28 Epidemiology of idiopathic generalized epilepsies Jallon P Epilepsia 2005 46 10 14 153
28 Long-term prognosis in two forms of childhood epilepsy: typical absence seizures and epilepsy with rolandic (centrotemporal) EEG foci Loiseau P Annals of Neurology 1983 13 642 648 153
31 Genome search for susceptibility loci of common idiopathic generalised epilepsies Sander T Human Molecular Genetics 2000 9 1465 1472 140
32 Reduced cortical inhibition in a mouse model of familial childhood absence epilepsy Tan HO Proceedings of the National Academy of Sciences of the United States of America 2007 104 17536 17541 136
33 Absence and myoclonic status epilepticus precipitated by antiepileptic drugs in idiopathic generalized epilepsy Thomas P Brain 2006 129 1281 1292 134
34 MRI volumetry of the thalamus in temporal, extratemporal, and idiopathic generalized epilepsy Natsume J Neurology 2003 60 1296 1300 129
34 Some clinical and EEG aspects of benign juvenile myoclonic epilepsy Asconape J Epilepsia 1984 25 108 114 129
36 Functional characterization and neuronal modeling of the effects of childhood absence epilepsy variants of CACNA1H, a T-type calcium channel Vitko I Journal of Neuroscience 2005 25 4844 4855 128
36 Frontal functions in juvenile myoclonic epilepsy Devinsky O Neuropsychiatry Neuropsychology and Behavioral Neurology 1997 10 243 246 128
38 Mapping of spontaneous spike and wave discharges in Wistar rats with genetic generalized nonconvulsive epilepsy Vergnes M Brain Research 1990 523 87 91 127
39 MR spectroscopy shows reduced frontal lobe concentrations of N-acetyl aspartate in patients with juvenile myoclonic epilepsy Savic I Epilepsia 2000 41 290 296 126
40 Genome scan of idiopathic generalized epilepsy: evidence for major susceptibility gene and modifying genes influencing the seizure type Durner M Annals of Neurology 2001 49 328 335 125
41 Voltage-gated calcium channels and idiopathic generalized epilepsies Khosravani H Physiological Reviews 2006 86 941 966 124
42 Do carbamazepine and phenytoin aggravate juvenile myoclonic epilepsy? Genton P Neurology 2000 55 1106 1109 123
42 Long-term prognosis of typical childhood absence epilepsy: remission or progression to juvenile myoclonic epilepsy Wirrell EC Neurology 1996 47 912 918 123
44 Gating effects of mutations in the Ca(v)3.2 T-type calcium channel associated with childhood absence epilepsy Khosravani H Journal of Biological Chemistry 2004 279 9681 9684 121
45 Ethosuximide, valproic acid, and lamotrigine in childhood absence epilepsy: initial monotherapy outcomes at 12 months Glauser TA Epilepsia 2013 54 141 155 119
46 Primary (idiopathic) generalized epilepsy and underlying mechanisms Niedermeyer E Clinical Electroencephalography 1996 27 1 21 118
47 Juvenile myoclonic epilepsy 25 years after seizure onset: a population-based study Camfield CS Neurology 2009 73 1041 1045 117
47 Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation Jones NC Experimental Neurology 2008 209 254 260 117
49 Quantitative MRI in patients with idiopathic generalized epilepsy. Evidence of widespread cerebral structural changes Woermann FG Brain 1998 121 1661 1667 116
49 Juvenile myoclonic epilepsy locus in chromosome 6p21.2-p11: linkage to convulsions and electroencephalography trait Liu AW American Journal of Human Genetics 1995 57 368 381 116
51 Extended spectrum of idiopathic generalized epilepsies associated with CACNA1H functional variants Heron SE Annals of Neurology 2007 62 560 568 115
52 Motor system hyperconnectivity in juvenile myoclonic epilepsy: a cognitive functional magnetic resonance imaging study Vollmar C Brain 2011 134 1710 1719 114
52 Voxel-based morphometry in patients with idiopathic generalized epilepsies Betting LE NeuroImage 2006 32 498 502 114
52 Mapping of genes predisposing to idiopathic generalized epilepsy Zara F Human Molecular Genetics 1995 4 1201 1207 114
55 BRD2 (RING3) is a probable major susceptibility gene for common juvenile myoclonic epilepsy Pal DK American Journal of Human Genetics 2003 73 261 270 113
56 From molecules to networks: cortical/subcortical interactions in the pathophysiology of idiopathic generalized epilepsy Blumenfeld H Epilepsia 2003 44 7 15 109
57 Cognitive function in idiopathic generalized epilepsy of childhood Henkin Y Developmental Medicine and Child Neurology 2005 47 126 132 107
58 Focal structural changes and cognitive dysfunction in juvenile myoclonic epilepsy O’Muircheartaigh J Neurology 2011 76 34 40 106
58 Childhood absence epilepsy and febrile seizures: a family with a GABA(A) receptor mutation Marini C Brain 2003 126 230 240 106
60 Hyperglycosylation and reduced GABA currents of mutated GABRB3 polypeptide in remitting childhood absence epilepsy Tanaka M American Journal of Human Genetics 2008 82 1249 1261 104
60 Reproducibility and complications in gene searches: linkage on chromosome 6, heterogeneity, association, and maternal inheritance in juvenile myoclonic epilepsy Greenberg DA American Journal of Human Genetics 2000 66 508 516 104
62 Clinical factors of drug resistance in juvenile myoclonic epilepsy Gelisse P Journal of Neurology Neurosurgery and Psychiatry 2001 70 240 243 102
63 Thalamofrontal circuitry and executive dysfunction in recent-onset juvenile myoclonic epilepsy Pulsipher DT Epilepsia 2009 50 1210 1219 100
63 Neuropsychological profile of patients with juvenile myoclonic epilepsy: a controlled study of 50 patients Pascalicchio TF Epilepsy and Behavior 2007 10 263 267 100
65 Genome-wide association analysis of genetic generalized epilepsies implicates susceptibility loci at 1q43, 2p16.1, 2q22.3 and 17q21.32 Steffens M Human Molecular Genetics 2012 21 5359 5372 98
66 Childhood absence epilepsy with tonic-clonic seizures and electroencephalogram 3-4-Hz spike and multispike-slow wave complexes: linkage to chromosome 8q24 Fong GCY American Journal of Human Genetics 1998 63 1117 1129 97
66 Linkage analysis of idiopathic generalized epilepsy (IGE) and marker loci on chromosome-6p in families of patients with juvenile myoclonic epilepsy: no evidence for an epilepsy locus in the HLA region Whitehouse WP American Journal of Human Genetics 1993 53 652 662 97
66 Juvenile myoclonic epilepsy: factors of error involved in the diagnosis and treatment Panayiotopoulos CP Epilepsia 1991 32 672 676 97
69 Clinical and EEG asymmetries in juvenile myoclonic epilepsy Lancman ME Epilepsia 1994 35 302 306 96
69 Juvenile myoclonic epilepsy: long-term response to therapy Penry JK Epilepsia 1989 30 S19 S23 96
71 Perampanel for tonic-clonic seizures in idiopathic generalized epilepsy. A randomized trial French JA Neurology 2015 85 950 957 95
71 Nerve fiber impairment of anterior thalamocortical circuitry in juvenile myoclonic epilepsy Deppe M Neurology 2008 71 1981 1985 95
73 Regional grey matter abnormalities in juvenile myoclonic epilepsy: a voxel-based morphometry study Kim JH NeuroImage 2007 37 1132 1137 93
73 The GABA(A) receptor gamma 2 subunit R43Q mutation linked to childhood absence epilepsy and febrile seizures causes retention of alpha 1 beta 2 gamma 2S receptors in the endoplasmic reticulum Kang JQ Journal of Neuroscience 2004 24 8672 8677 93
73 Magnetic resonance spectroscopy and imaging of the thalamus in idiopathic generalized epilepsy Bernasconi A Brain 2003 126 2447 2454 93
76 Impaired attention and network connectivity in childhood absence epilepsy Killory BD NeuroImage 2011 56 2209 2217 92
76 The relationship between treatment with valproate, lamotrigine, and topiramate and the prognosis of the idiopathic generalised epilepsies Nicolson A Journal of Neurology Neurosurgery and Psychiatry 2004 75 75 79 92
78 Thalamo-cortical network pathology in idiopathic generalized epilepsy: insights from MRI-based morphometric correlation analysis Bernhardt BC NeuroImage 2009 46 373 381 91
78 Why does fever trigger febrile seizures? GABA(A) receptor gamma 2 subunit mutations associated with idiopathic generalized epilepsies have temperature-dependent trafficking deficiencies Kang JQ Journal of Neuroscience 2006 26 2590 2597 91
78 Focal electroencephalographic abnormalities in juvenile myoclonic epilepsy Aliberti V Epilepsia 1994 35 297 301 91
78 Juvenile myoclonic epilepsy: a study in Saudi Arabia Obeid T Epilepsia 1988 29 280 282 91
82 Pretreatment cognitive deficits and treatment effects on attention in childhood absence epilepsy Masur D Neurology 2013 81 1572 1580 88
82 Electroclinical features of absence seizures in childhood absence epilepsy Sadleir LG Neurology 2006 67 413 418 88
82 Genetic architecture of idiopathic generalized epilepsy: clinical genetic analysis of 55 multiplex families Marini C Epilepsia 2004 45 467 478 88
82 Juvenile myoclonic epilepsy. A review Grunewald RA Archives of Neurology 1993 50 594 598 88
86 Juvenile myoclonic epilepsy subsyndromes: family studies and long-term follow-up Martinez-Juarez IE Brain 2006 129 1269 1280 86
87 Proton MRS reveals frontal lobe metabolite abnormalities in idiopathic generalized epilepsy Simister RJ Neurology 2003 61 897 902 85
88 Exacerbation of juvenile myoclonic epilepsy with lamotrigine Biraben A Neurology 2000 55 1758 1758 84
89 Multi-site voxel-based morphometry: methods and a feasibility demonstration with childhood absence epilepsy Pardoe H NeuroImage 2008 42 611 616 83
89 Delayed diagnosis of juvenile myoclonic epilepsy Grunewald RA Journal of Neurology Neurosurgery and Psychiatry 1992 55 497 499 83
91 The idiopathic generalized epilepsies of adolescence with childhood and juvenile age of onset Janz D Epilepsia 1997 38 4 11 82
92 Glucose transporter 1 deficiency in the idiopathic generalized epilepsies Arsov T Annals of Neurology 2012 72 807 815 81
93 Idiopathic generalized epilepsies recognized by the International League Against Epilepsy Nordli DR Epilepsia 2005 46 48 56 80
94 Genome arrays for the detection of copy number variations in idiopathic mental retardation, idiopathic generalized epilepsy and neuropsychiatric disorders: lessons for diagnostic workflow and research Hochstenbach R Cytogenetic and Genome Research 2011 135 174 202 79
94 The I-II loop controls plasma membrane expression and gating of Ca(v)3.2 T-type Ca2+ channels: a paradigm for childhood absence epilepsy mutations Vitko I Journal of Neuroscience 2007 27 322 330 79
96 Sleep microstructure and EEG epileptiform activity in patients with juvenile myoclonic epilepsy Gigli GL Epilepsia 1992 33 799 804 78
96 Juvenile myoclonic epilepsy: an autosomal recessive disease Panayiotopoulos CP Annals of Neurology 1989 25 440 443 78
98 Thalamic atrophy in childhood absence epilepsy Chan CH Epilepsia 2006 47 399 405 76
98 Worsening of seizures by oxcarbazepine in juvenile idiopathic generalized epilepsies Gelisse P Epilepsia 2004 45 1282 1286 76
98 Tiagabine-induced absence status in idiopathic generalized epilepsy Knake S Seizure - European Journal of Epilepsy 1999 8 314 317 76

GGE, genetic generalized epilepsy; GABA, gamma-Aminobutyric acid; JME, Juvenile myoclonic epilepsy; Bf, factor B; HLA, human leukocyte antigen; IGE, idiopathic generalized epilepsy; fMRI, functional magnetic resonance imaging; CLCN2, chloride voltage-gated channel 2; CACNB4, calcium voltage-gated channel auxiliary subunit beta 4; EEFHC1, EF-hand domain containing 1; GABRG2, gamma-Aminobutyric Acid type A receptor subunit gamma 2; EEG, electroencephalography; MRI, magnetic resonance imaging; RING3, Really Interesting New Gene 3; MRS, MR spectroscopy.

Table 2.
Journals containing at least 2 of the top-100 cited articles in the field of GGE
Rank Journal Number of articles
1 Epilepsia 19
2 Neurology 15
3 Brain 10
4 American Journal of Human Genetics 6
4 Annals of Neurology 6
4 NeuroImage 6
7 Human Molecular Genetics 5
7 Nature Genetics 5
9 Journal of Neurology Neurosurgery and Psychiatry 4
9 Journal of Neuroscience 4
11 American Journal of Medical Genetics 3
12 Archives of Neurology 2

GGE, genetic generalized epilepsy.

Table 3.
Countries of origin of the top-100 cited articles in the field of GGE
Rank Country Number of articles
1 USA 31
2 UK 14
3 Germany 11
3 Australia 11
5 France 7
6 Canada 9
7 Saudi Arabia 3
8 Italy 2
8 Brazil 2
8 Netherlands 2
8 China 2
12 Switzerland 1
12 New Zealand 1
12 South Korea 1
12 Sweden 1
12 Israel 1
12 Japan 1

GGE, genetic generalized epilepsy.

Table 4.
Originating institutions with at least 2 of the top-100 cited articles in the field of GGE
Rank Institution Number of articles
1 University of Melbourne 9
2 University of California at Los Angeles 7
3 University College London 6
4 University of McGill 5
5 University of New York 4
6 University of King Khalid 3
6 University of Humboldt 3
6 King’s College London 3
9 University of Saint Paul 2
9 University of Calgary 2
9 University of Cincinnati 2
9 University of Virginia 2
9 University of Wake Forest 2
9 University of Vanderbilt 2

GGE, genetic generalized epilepsy.

Table 5.
First authors with at least 2 of the top-100 cited articles in the field of GGE
Rank First author Number of articles
1 Panayiotopoulos CP 3
2 Dumer M 2
2 Gelisse P 2
2 Glauser TA 2
2 Greengerg DA 2
2 Grunewald RA 2
2 Janz D 2
2 Kang JQ 2
2 Khosravani H 2
2 Marini C 2
2 Vitko I 2
2 Woermann FG 2

GGE, genetic generalized epilepsy.

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