Top-100 cited articles on Guillain-Barré syndrome: a bibliometric analysis

Running title: Top-100 articles on GBS

Jee-Eun Kim,1* Jong Kuk Kim2*, Kang Min Park3, Yerim Kim4, Dae Young Yoon5, Jong Seok
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Bae4
1
Department of Neurology, Seoul Medical Center, Seoul, Korea
2
Department of Neurology, Dong-A University College of Medicine, Busan, Korea
3
Department of Neurology, Haeundae Paik Hospital, Inje University College of Medicine,
Busan, Korea
4
Department of Neurology, Kangdong Sacred Heart Hospital, Hallym University College of
Medicine, Seoul, Korea
5
Department of Radiology, Kangdong Sacred Heart Hospital, Hallym University College of
Medicine, Seoul, Korea

*These authors contributed equally to this work.

Corresponding author: Jong Seok Bae, M.D., Ph.D.

Address: Department of Neurology, Kangdong Sacred Heart Hospital, Hallym University
College of Me dicine, 150 Seongan-ro, Gangdong-gu, Seoul 134-701, Korea

Tel.: +82-2-22242854, Fax: +82-2-4786330, Email: lwsbae@naver.com (J.S.B.)

Acknowledgements

This work was supported by a Dong-A University research fund (J.K.K.). J.S.B. Y.D.Y.
designed the study. J.S.B., J.E.K., and J.K.K. conducted the data collection. J.S.B., Y.D.Y.,
J.E.K., J.K.K., K.M.P., and Y.K. interpreted the data, reviewed the first manuscript draft,
critically revised the manuscript, and read and approved the final version of the manuscript.

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which
may lead to differences between this version and the Version of Record. Please cite this
article as doi: 10.1111/jns.12188

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 Abstract

Since the first description of Guillain-Barré syndrome (GBS) 100 years ago, the concept of

this syndrome has changed remarkably. The purpose of our study was to identify and
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characterize the most-cited articles that have contributed to advancing the understanding of

GBS. Based on the database of Journal Citation Reports, we selected 554 journals that were

considered as potential sources of reports on studies related to clinical neurology and general

medicine. The Web of Science search tools were used to identify the most-cited articles

relevant to GBS or other variants in the selected journals. Of the selected articles, 18 were

review articles and the remainder were original articles or included only a few case series.

Among the original articles, 13 described basic research associated with immunological

pathogenesis involving anti-ganglioside antibodies. Most of the original studies (42/64, 66%)

published after 1990 evaluated anti-ganglioside antibodies that mediated axonal GBS or

Miller Fisher syndrome, with only a small number of the papers involving electrodiagnostic

medicine (n=4). Our bibliometric analysis has yielded a detailed list of the top-100 cited

articles in the field of GBS.

Keywords: bibliometric analysis; citation; citation classics; Guillain-Barré syndrome

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 Introduction

Guillain-Barré syndrome (GBS) is a prototype postinfectious acute peripheral

neuropathy that is now one of the leading causes of flaccid paralysis (Bae et al., 2014; Yuki
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and Hartung, 2012). Since the first description of GBS 100 years ago (Guillain et al., 1916),

there have been remarkable advances in the understanding of this unique syndrome. GBS is

now understood to be an inflammatory peripheral neuropathy attributable to antecedent

infections or other immunogenic events (Bae et al., 2014; Yuki and Hartung, 2012). GBS is

generally subclassified by both the pathological involvement and phenotypical distinction of

each subtype.

The present study identified the most-cited articles related to GBS research and analyzed

the trends in these articles according to the evolution of GBS and our own understanding of

this unique and rare syndrome.

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 Materials and Methods

We performed a search of journals and selected the most-cited articles by utilizing the

Institute for Scientific Information (ISI) Web of Science (Thomson Reuters, New York, NY)
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database. Based on Journal Citation Reports (Thomson Reuters) Science Edition 2014, the

following three subject categories of journals were included: 192 journals on clinical

neurology, 252 journals on “neuroscience, and 110 journals on “medicine, general & internal.”

For each included journal, we retrieved all articles that were cited more than 100 times

at the time of the search (February 2016) using the “cited reference search” facility of the

Science Citation Index Expanded of the ISI Web of Science. The ISI Web of Science is a

multidisciplinary database providing the most relevant bibliometric information from

published scientific articles since 1950; it fully indexes more than 8600 major journals across

176 subject categories.

To identify frequently cited GBS-specific articles, we searched the following terms

either singly or in combination in the selected articles that had been cited more than 100

times: “Guillain-Barré syndrome,” “acute inflammatory demyelinating polyneuropathy or

polyradiculoneuropathy,” “acute motor axonal neuropathy,” “acute motor sensory axonal

neuropathy,” “Miller Fisher syndrome,” “Fisher syndrome,” “acute sensory ataxic

neuropathy,” “pharyngeal-cervical-brachial variant,” “facial diplegia with paresthesia,”

“antibodies against the gangliosides GM1, GM2, GD1a, GD1b, GD3, GT1a, GT1b, N-

acetylgalactosaminyl (GalNAc) GD1a, and GQ1b,” “nodopathy,” “paranodopathy,” and

“reversible conduction failure/block. Additionally, two neurologists (J.S.B. and J.E.K.)

manually reviewed the contents of articles independently. If there were any arguments

between those two authors in the selections, another two neurologists (J.K.K. and K.M.P.)

finally confirmed the selections.

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 This procedure resulted in the top-100 cited articles being selected and reviewed. The

following information about these articles was extracted: (i) year of publication, (ii) journal

title, (iii) journal category (clinical neurology or clinical neuroscience; basic neuroscience;
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general medicine or interdisciplinary), (iv) number of citations, (v) authorship, (vi) authors’

affiliations, (vii) authors’ nationalities, (viii) article type (original article [clearly stated

objectives or hypotheses and containing specifically articulated methods and results sections],

review article, case series, or systematic review/meta-analysis), (ix) topic categories (clinical

research, therapeutic trial, immunological study, pathology, or other), and (x) subjects

analyzed (e.g., GBS, AMAN, MFS, or other subtypes of GBS).

When the authors of an article had more than one affiliation, the department, institution,

and country of origin were defined by the affiliation of the corresponding author. Data are

presented using descriptive statistics, and no tests of statistical significance were performed.

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 Results

We finally selected and analyzed 102 articles that were cited more than 100 times as

citation classics of GBS. Being cited more than 400 times has previously been defined as a
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citation classic, although in some fields with fewer researchers a threshold of 100 citations

has been considered sufficient (Garfield, Accessed on April 30, 2016). Since GBS is a very

rare disease, with a reported incidence in Western countries ranging from 0.89 to 1.89 cases

(median, 1.11) per 100,000 person-years (Bae et al., 2014; Yuki and Hartung, 2012), we

decided that any GBS publication with more than 100 citations should be considered to be a

citation classic.

The top-10 cited classics included two randomized clinical trials for immunotherapies (1,

8) and four review articles on clinical aspects of GBS (2, 3, 4, 6b; the parenthesized numbers

here and below refer to the rank in Table 1). Landmark studies that provided the turning point

for GBS pathophysiology were also nominated as the top-10 classics: the introduction of

axonal GBS (10), typical examples of AMAN from northern China (5), the relationship

between C. jejuni and AMAN (9), and anti-GQ1b antibody as the pathogenic antibody for

MFS (6a). These 10 articles led to the novel concept of axonal GBS and its immune-mediated

pathogenesis.

In total, 102 articles on GBS were identified as being cited more than 100 times, while

the top-10 articles were cited more than 400 times. We consider the top-100 cited articles to

be GBS citation classics (Table 1). The top-ranked article was authored by Van der Meché

and Schmitz in 1992, and reported on a randomized trial of main two treatments of GBS (van

der Meche and Schmitz, 1992). The journal that published GBS citation classics most

frequently was “Annals of Neurology,” followed by “Neurology” and “Brain.” About 80% of

the journals were related to clinical neurology, with the remainder being related to general

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 medicine (Table 2). The affiliations of about half of the authors of the GBS citation classics

were in the United States of America followed by Japan and the United Kingdom (Table 3).

Tables 4 and 5 list the top-ranked institutions and authors for the published GBS citation
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classics. The institutions associated with the largest number of GBS citation classics were

Erasmus University (Department of Neurology) in the Netherlands and Johns Hopkins

School of Medicine (Department of Neurology) in the United States of America. Cornblath

DR is the author listed most frequently in the GBS citation classics.

The years of publication were concentrated in the 1990s, with about half of the top-100

citation classics being published during 1992–1998 and 61 of them being published

throughout the 1990s (Fig. 1).

Regarding the type of articles, 18 were review articles and the remainder were original

articles or included only a few case series. Four of the review articles were specifically

focused on diagnostic considerations and subclassification of GBS (3, 15, 96c, 100). With the

evolution of the GBS concept, these citation classics summarized the contemporary status of

a diagnosis of GBS during the 1980s, 1990s, and 2000s. Two review articles specifically

considered the therapeutic subject: one article reported on a systematic review (67b) and the

other provided practical parameter for therapeutic guidance (99).

Among the original articles, 13 described basic research studies. Most of them had

investigated the immunological pathogenesis associated with various types of gangliosides

(GM1, GQ1b, GD1b, GD1a, and GalNAc-GD1a). As landmark studies, the existence of

axonal GBS was first suggested by Feasby and colleagues (10). This was subsequently

confirmed pathologically in clustered patients from northern China (5, 11). Most of the

original studies (42/64, 66%) published after 1990 evaluated anti-ganglioside antibodies

mediated GBS or axonal GBS. One study established an animal model of AMAN (35).

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 Three randomized controlled trials focusing on the therapeutic aspect were identified

among the 100 citation classics (1, 8, 71) for the immunotherapy of GBS. Recent review

articles have addressed the immunobiology of axonal GBS (e.g., 94b).

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Only nine studies were related to MFS or the anti-GQ1b antibody, and one study

addressed Bickerstaff brainstem encephalitis. Of these, the Chiba and Kusunoki group

identified anti-GQ1b antibody as the pathogenic marker of MFS in the two highest-ranked

studies of MFS (6a, 12). Only two studies had performed an epidemiological survey of GBS

(47, 72c), Rees and coworkers demonstrated that AIDP is more common in Western countries

(47). An unexpected finding is that only a few studies focused on the electrophysiological

criteria were identified as citation classics. Most of the frequently used electrophysiological

criteria were arbitrarily defined in each clinical study (13, 41b, 72a, 89, 100).

The two most frequently utilized electrodiagnostic criteria of GBS were reported by Ho

and colleagues (5) and Hadden and colleagues (13). The traditional electrophysiological

criteria were recently criticized for discriminating between axonal and demyelinating GBS

because of reversible conduction failure. The study by Kuwabara and colleagues (41b) started

the controversy regarding the need to revise the electrophysiological criteria of GBS and the

recent concept of axonal GBS, so-called nodo-/paranodopathy (Uncini and Kuwabara, 2012;

Uncini and Kuwabara, 2015; Uncini et al., 2010).

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 Discussion

The list of the top-100 most-cited articles in Table 1 presents the authors and the topics

that reflect the main advances in GBS research in the fields of neuroimmunology,
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experimental investigations, epidemiology, and electrophysiology, as well as clinical studies

during the last 60 years. The concept and classification of GBS have changed remarkably

during the last 3 decades, with the most notable advance being the identification of an axonal

variant of GBS (Bae et al., 2014; Yuki and Hartung, 2012; Yuki and Kuwabara, 2007). This

advance arose chiefly through studies undertaken in East Asian countries, which

demonstrated the relationship between anti-ganglioside antibodies and axonal GBS, such as

AMAN (Ho et al., 1995; McKhann et al., 1993; Yuki and Kuwabara, 2007). Most of these

studies were prompted by the introduction of the concept of axonal GBS (Feasby et al., 1986),

proof of axonal pathology (Ho et al., 1995; McKhann et al., 1993), and the pathogenic role of

anti-ganglioside antibodies (Ilyas et al., 1988). Some of these studies analyzed Chinese

patients, thereby revealing the presence of geographic differences in the incidence of axonal

GBS (Bae et al., 2014; Rees et al., 1998).

Articles published before the axonal GBS concept was introduced—generally before

1990—were less frequently ranked as GBS citation classics. This also reflects that basic and

clinical studies of AIDP were cited less frequently and probably also conducted less

frequently in the past. Given that AIDP was used as a synonym of GBS for an extended

period, with this term defining clinicopathological aspects of GBS, this has affected the

recent trends in GBS research (Bae et al., 2014).

Many of the citation classics focused on the pathophysiological aspects of axonal GBS.

Therapeutic trials and epidemiological studies have been cited less frequently in research

fields related to GBS. In summary, the most distinct finding of our analysis was axonal GBS

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 being the main focus in the citation classics. Identifying this trend provides clear insights into

the revolutionary changes of the disease concept and the understanding that clinicians have

had about GBS during the last 30 years.

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Several limitations of our bibliometric analysis need to be considered, including several

inherent limitations that have been highlighted in previous bibliometric analyses using similar

methods. First, the overall number of citations of an article is likely to be influenced by its

publication year. (Pepe and Kurtz, 2012) Older articles have more chances to be cited than

recently published ones, because citations usually accumulate over time. However, time

factor might also reversely influence the citation number of older works since there were less

citations before 1990 and total number of GBS related articles exponentially increased after

1990. Second, retrieving the GBS related journals only in the categories of “clinical

neurology”, “neuroscience” and “medicine, general & internal” in ISI Web of Science

database, might have missed some significant articles that are included in other sections as

“immunology”, “medicine, research & experimental”, etc. Third, the number of citations can

be influenced by not only the quality of the article but also by factors such as obliteration by

incorporation (i.e., the phenomenon that information from highly influential articles has been

incorporated into common knowledge so that they no longer need to be cited explicitly),

omission bias (i.e., the tendency to not cite competitors or sources contradictory to one’s own

results), self-citation, referencing high-IF core journals in the field of study, preference to cite

review articles over original research, and country or language preferences (Braun, 2003;

Dumont, 1989).

A strength of our study was that we compiled a comprehensive list of the most-cited

GBS articles across all relevant peer-reviewed scientific journals. By analyzing a total of 554

journals on clinical neurology, neuroscience, and medicine, general & internal, we identified

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 all classic articles published in specialist neurology and neuroscience journals as well as

high-IF interdisciplinary journals. We identified and bibliometrically analyzed the top-100

cited articles in the field of GBS.

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2016 is a particularly meaningful year since it is the centennial of the first

conceptualization of GBS by pioneers of this unique syndrome: Guillain G, Barré JA, and

Strohl A. Our list of the top-100 cited articles provides insight into historical developments

and recognizes important advances in the field of a prototype of acute immune-mediated

peripheral neuropathy.

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 References

Bae JS, Yuki N, Kuwabara S, Kim JK, Vucic S, Lin CS, Kiernan MC (2014). Guillain-Barre

syndrome in Asia. Journal of neurology, neurosurgery, and psychiatry 85:907-913.

Accepted Article
Braun T (2003). The reliability of total citation rankings. J Chem Inf Comput Sci 43:45-46.

Dumont JE (1989). The bias of citations. Trends Biochem Sci 14:327-328.

Feasby TE, Gilbert JJ, Brown WF, Bolton CF, Hahn AF, Koopman WF, Zochodne DW (1986).

An acute axonal form of Guillain-Barre polyneuropathy. Brain 109 ( Pt 6):1115-1126.

Garfield E (Accessed on April 30, 2016). What is a citation classic? In: Citation classics.

Guillain G, Barré JA, Strohl A (1916). Sur un syndrome de radiculonévrite avec

hyperalbuminose du liquide céphalo-rachidien sans réaction cellulaire. Remarques sur les

caractères cliniques et graphiques des réflexes tendineux [French]. Bull Mem Hop Paris

40:1462–1470.

Ho TW, Mishu B, Li CY, Gao CY, Cornblath DR, Griffin JW, Asbury AK, Blaser MJ,

McKhann GM (1995). Guillain-Barré syndrome in northern China. relationship to

Campylobacter jejuni infection and anti-glycolipid antibodies. Brain 118:597-605.

Ilyas AA, Willison HJ, Quarles RH, Jungalwala FB, Cornblath DR, Trapp BD, Griffin DE,

Griffin JW, McKhann GM (1988). Serum antibodies to gangliosides in Guillain-Barre

syndrome. Ann Neurol 23:440-447.

McKhann GM, Cornblath DR, Griffin JW, Ho TW, Li CY, Jiang Z, Wu HS, Zhaori G, Liu Y,

Jou LP, et al. (1993). Acute motor axonal neuropathy: a frequent cause of acute flaccid

paralysis in China. Ann Neurol 33:333-342.

Pepe A, Kurtz MJ (2012). A measure of total research impact independent of time and

discipline. PLoS One 7:e46428.

Rees JH, Thompson RD, Smeeton NC, Hughes RA (1998). Epidemiological study of

This article is protected by copyright. All rights reserved.

 Guillain-Barre syndrome in south east England. Journal of neurology, neurosurgery, and

psychiatry 64:74-77.

Uncini A, Kuwabara S (2012). Electrodiagnostic criteria for Guillain-Barré syndrome: a

Accepted Article
critical revision and the need for an update. Clin Neurophysiol 123:1487-1495.

Uncini A, Kuwabara S (2015). Nodopathies of the peripheral nerve: an emerging concept.

Journal of neurology, neurosurgery, and psychiatry 86:1186-1195.

Uncini A, Manzoli C, Notturno F, Capasso M (2010). Pitfalls in electrodiagnosis of Guillain-

Barré syndrome subtypes. Journal of neurology, neurosurgery, and psychiatry 81:1157-1163.

van der Meche FG, Schmitz PI (1992). A randomized trial comparing intravenous immune

globulin and plasma exchange in Guillain-Barre syndrome. Dutch Guillain-Barre Study

Group. The New England journal of medicine 326:1123-1129.

Yuki N, Hartung HP (2012). Guillain-Barre syndrome. The New England journal of medicine

366:2294-2304.

Yuki N, Kuwabara S (2007). Axonal Guillain-Barré syndrome: carbohydrate mimicry and

pathophysiology. J Peripher Nerv Syst 12:238-249.

This article is protected by copyright. All rights reserved.

 Tables

Table 1. The top-100 cited articles on GBS.

Rank Article Number

Accepted Article
of
citations
Van der Meché FG, Schmitz PI. A randomized trial comparing
1 intravenous immune globulin and plasma exchange in Guillain-Barré 812
syndrome. N Engl J Med 1992;326:1123-9.
Hughes RA, Cornblath DR. Guillain-Barré syndrome. Lancet
2 616
2005;366:1653-66.
Asbury AK, Cornblath DR. Assessment of current diagnostic criteria
3 611
for Guillain-Barré syndrome. Ann Neurol 1990;27:S21-4.
Haymaker WE, Kernohan JW. The Landry-Guillain-Barré syndrome;
4 a clinicopathologic report of 50 fatal cases and a critique of the 460
literature. Medicine 1949;28:59-141.
Ho TW, Mishu B, Li CY, et al. Guillain-Barré syndrome in northern
5 China. Relationship to Campylobacter jejuni infection and anti- 444
glycolipid antibodies. Brain 1995;118:597-605.
Chiba A, Kusunoki S, Obata H, et al. Serum anti-GQ1b IgG antibody
is associated with ophthalmoplegia in Miller Fisher syndrome and
6a 430
Guillain-Barré syndrome: clinical and immunohistochemical studies.
Neurology 1993;43:1911-7.
Ropper AH. The Guillain-Barré syndrome. N Engl J Med
6b 430
1992;326:1130-6.
Hughes RAC, Swan AV, Cornblath DR, et al. Randomised trial of
8 plasma exchange, intravenous immunoglobulin, and combined 426
treatments in Guillain-Barré syndrome. Lancet 1997;349;225-30.
Rees JH, Soudain SE, Gregson NA, et al. Campylobacter jejuni
9 infection and Guillain-Barré syndrome. N Engl J Med 424
1995;333:1374-9.
Feasby TE, Gilbert JJ, Brown WF, et al. An acute axonal form of
10 404
Guillain Barré polyneuropathy. Brain 1986;109:1115-26.
McKhann GM, Cornblath DR, Griffin JW, et al. Acute motor axonal
11 neuropathy: a frequent cause of acute flaccid paralysis in China. Ann 384
Neurol 1993;33:333-42.

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 Chiba A, Kusunoki S, Shimizu T, et al. Serum IgG antibody to
12 ganglioside GQ1b is a possible marker of Miller Fisher syndrome. 356
Ann Neurol 1992;31:677-9.
Hadden RD, Cornblath DR, Hughes RA, et al. Electrophysiological
13 classification of Guillain-Barré syndrome: clinical associations and 352
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outcome. Ann Neurol 1998;44:780-8.
Jacobs BC, Rothbarth PH, van der Meché FG, et al. The spectrum of
14 antecedent infections in Guillain-Barré syndrome: a case-control 326
study. Neurology 1998;51:1110-5.
Asbury AK. Diagnostic considerations in Guillain-Barré syndrome.
15 315
Ann Neurol 1981;9:1-5.
Lasky T, Terracciano GJ, Magder L, et al. The Guillain-Barré
16 syndrome and the 1992-1993 and 1993-1994 influenza vaccines. N 296
Engl J Med 1998;339:1797-802.
Kleyweg RP, van der Meché FG, Schmitz PI. Interobserver
17 agreement in the assessment of muscle strength and functional 265
abilities in Guillain-Barré syndrome. Muscle Nerve 1991;14:1103-9.
Hafer-Macko C, Hsieh ST, Li CY, et al. Acute motor axonal
18 neuropathy: an antibody-mediated attack on axolemma. Ann Neurol 262
1996;40:635-44.
Griffin JW, Li CY, Ho TW, et al. Guillain-Barré syndrome in northern
19 China. The spectrum of neuropathological changes in clinically 256
defined cases. Brain 1995;118:577-95.
Griffin JW, Li CY, Ho TW, et al. Pathology of the motor-sensory
20 253
axonal Guillain-Barré syndrome. Ann Neurol 1996;39:17-28.
Hartung HP, Pollard JD, Harvey GK, et al. Immunopathogenesis and
21 treatment of the Guillain-Barré syndrome--Part I. Muscle Nerve 252
1995;18:137-53.
Brown WF, Feasby TE. Conduction block and denervation in
22 247
Guillain-Barré polyneuropathy. Brain 1984;107:219-39.
van Doorn PA, Ruts L, Jacobs BC. Clinical features, pathogenesis,
23 and treatment of Guillain-Barré syndrome. Lancet Neurol 236
2008;7:939-50.
24 Hahn AF. Guillain-Barré syndrome. Lancet 1998;352:635-41. 235
Ilyas AA, Willison HJ, Quarles RH, et al. Serum antibodies to
25 219
gangliosides in Guillain-Barré syndrome. Ann Neurol 1988;23:440-7.

This article is protected by copyright. All rights reserved.

 Willison HJ, Veitch J, Paterson G, et al. Miller Fisher syndrome is
26 associated with serum antibodies to GQ1b ganglioside. J Neurol 213
Neurosurg Psychiatry 1993;56:204-6.
Jacobs BC, van Doorn PA, Schmitz PI, et al. Campylobacter jejuni
27 infections and anti-GM1 antibodies in Guillain-Barré syndrome. Ann 211
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Neurol 1996;40:181-7.
Rees JH, Gregson NA, Hughes RA. Anti-ganglioside GM1 antibodies
28 in Guillain-Barré syndrome and their relationship to Campylobacter 204
jejuni infection. Ann Neurol 1995;38:809-16.
Kuroki S, Saida T, Nukina M, et al. Campylobacter jejuni strains
from patients with Guillain-Barré syndrome belong mostly to Penner
29a 198
serogroup 19 and contain beta-N-acetylglucosamine residues. Ann
Neurol 1993;33:243-7.
McKhann GM, Griffin JW, Cornblath DR, et al. Plasmapheresis and
29b Guillain-Barré syndrome: analysis of prognostic factors and the effect 198
of plasmapheresis. Ann Neurol 1988;23:347-53.
Raphael JC, Chastang C, Jais J-P,et al. Efficiency of plasma exchange
31 in Guillain-Barré syndrome: role of replacement fluids. Ann Neurol 196
1987;22:753-61.
Hafer-Macko CE, Sheikh KA, Li CY, et al. Immune attack on the
32 Schwann cell surface in acute inflammatory demyelinating 191
polyneuropathy. Ann Neurol 1996;39:625-35.
Ho TW, Willison HJ, Nachamkin I, et al. Anti-GD1a antibody is
33 associated with axonal but not demyelinating forms of Guillain-Barré 190
syndrome. Ann Neurol 1999;45:168-73.
Ogawara K, Kuwabara S, Mori M, et al. Axonal Guillain-Barré
34 syndrome: relation to anti-ganglioside antibodies and Campylobacter 189
jejuni infection in Japan. Ann Neurol 2000;48:624-31.
Yuki N, Yamada M, Koga M, et al. Animal model of axonal Guillain-
35 Barré syndrome induced by sensitization with GM1 ganglioside. Ann 178
Neurol 2001;49:712-20.
Kleyweg RP, van der Meché FG, Meulstee J. Treatment of Guillain-
36a Barré syndrome with high-dose gammaglobulin. Neurology 175
1988;38:1639-41.
Prineas JW. Pathology of the Guillain Barré syndrome. Ann Neurol
36b 175
1981;9:6-19.

38a Hadden RD, Karch H, Hartung HP, et al. Preceding infections, 172
immune factors, and outcome in Guillain-Barré syndrome. Neurology

This article is protected by copyright. All rights reserved.

 2001;56:758-65.

Lichtenfeld P. Autonomic dysfunction in the Guillain Barré

38b 172
syndrome. Am J Med 1971;50:772-80.
Yuki N, Sato S, Tsuji S, et al. Frequent presence of anti-GQ1b
40 166
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antibody in Fisher's syndrome. Neurology 1993;43:414-7.
Al-Din AN, Anderson M, Bickerstaff ER, et al. Brainstem
41a encephalitis and the syndrome of Miller Fisher: a clinical study. Brain 164
1982;105:481-95.
Kuwabara S, Yuki N, Koga M, et al. IgG anti-GM1 antibody is
41b associated with reversible conduction failure and axonal degeneration 164
in Guillain-Barré syndrome. Ann Neurol 1998;44:202-8.
Lisak RP, Mitchell M, Zweiman B, et al. Guillain-Barré syndrome
41c and Hodgkin's disease: three cases with immunological studies. Ann 164
Neurol 1977;1:72-8.
Enders U, Karch H, Toyka KV, et al. The spectrum of immune
responses to Campylobacter jejuni and glycoconjugates in Guillain-
44 162
Barré syndrome and in other neuroimmunological disorders. Ann
Neurol 1993;34:136-44.
Odaka M, Yuki N, Yamada M, et al. Bickerstaff's brainstem
45 encephalitis: clinical features of 62 cases and a subgroup associated 159
with Guillain-Barré syndrome. Brain 2003;126:2279-90.
Susuki K, Rasband MN, Tohyama K, et al. Anti-GM1 antibodies
46 cause complement-mediated disruption of sodium channel clusters in 158
peripheral motor nerve fibers. J Neurosci 2007;27:3956-67.
Rees JH, Thompson RD, Smeeton NC, et al. Epidemiological study
47 of Guillain-Barré syndrome in south east England. J Neurol 156
Neurosurg Psychiatry 1998;64:74-7.
Chiba A, Kusunoki S, Obata H, et al. Ganglioside composition of the
48 human cranial nerves, with special reference to pathophysiology of 155
Miller Fisher syndrome. Brain Res 1997;745:32-6.
van Koningsveld R, Schmitz PI, Meché FG, et al. Effect of
methylprednisolone when added to standard treatment with
49 152
intravenous immunoglobulin for Guillain-Barré syndrome:
randomised trial. Lancet 2004;363:192-6.
Roberts M, Willison H, Vincent A, et al. Serum factor in Miller-
50 Fisher variant of Guillain-Barré syndrome and neurotransmitter 148
release. Lancet 1994;343:454-5.

This article is protected by copyright. All rights reserved.

 Cook SD, Dowling PC. The role of autoantibody and immune
51 complexes in the pathogenesis of Guillain-Barré syndrome. Ann 146
Neurol 1981;9:70-9.
Plomp JJ, Molenaar PC, O'Hanlon GM, et al. Miller Fisher anti-
52 GQ1b antibodies: alpha-latrotoxin-like effects on motor end plates. 145
Accepted Article
Ann Neurol 1999;45:189-99.
Mishu B, Ilyas AA, Koski CL, et al. Serologic evidence of previous
53a Campylobacter jejuni infection in patients with the Guillain-Barré 143
syndrome. Ann Intern Med 1993;118:947-53.
Visser LH, Van der Meché FG, Van Doorn PA, et al. Guillain-Barré
syndrome without sensory loss (acute motor neuropathy). A subgroup
53b 143
with specific clinical, electrodiagnostic and laboratory features. Brain
1995;118:841-7.
Haber P, DeStefano F, Angulo FJ, et al. Guillain-Barré syndrome
55a 141
following influenza vaccination. JAMA 2004;292:2478-81.
Ropper AH. Unusual clinical variants and signs in Guillain-Barré
55b 141
syndrome. JAMA Neurol 1986;43:1150-2.

Yuki N, Hartung HP. Medical progress: Guillain Barré syndrome. N

57 140
Engl J Med 2012; 366:2294-304

Mori M, Kuwabara S, Fukutake T, et al. Clinical features and

58 139
prognosis of Miller Fisher syndrome. Neurology 2001;56:1104-6.
Kusunoki S, Shimizu J, Chiba A, et al. Experimental sensory
59a neuropathy induced by sensitization with ganglioside GD1b. Ann 138
Neurol 1996;39:424-31.
Vriesendorp FJ, Mishu B, Blaser MJ, et al. Serum antibodies to GM1,
GD1b, peripheral nerve myelin, and Campylobacter jejuni in patients
59b 138
with Guillain-Barré syndrome and controls: correlation and
prognosis. Ann Neurol 1993;34:130-5.
Leneman F. The Guillain-Barré syndrome. Definition, etiology, and
61 137
review of 1,100 cases. JAMA Intern Med 1966;118:139-44.
Dowling PC, Cook SD. Role of infection in Guillain-Barré syndrome:
62 laboratory confirmation of herpesviruses in 41 cases. Ann Neurol 136
1981;9:44-55.
Kusunoki S, Chiba A, Kon K, et al. N-acetylgalactosaminyl GD1a is
63 a target molecule for serum antibody in Guillain-Barré syndrome. 135
Ann Neurol 1994;35:570-6.

64a Hartung HP, Hughes RA, Taylor WA, et al. T cell activation in 134

This article is protected by copyright. All rights reserved.

 Guillain-Barré syndrome and in MS: elevated serum levels of soluble
IL-2 receptors. Neurology 1990;40:215-8.
Wiederholt WC, Mulder DW, Lambert EH. The Landry-Guillain-
Barré-Strohl syndrome or polyradiculoneuropathy: historical review,
64b 134
report on 97 patients, and present concepts. Mayo Clin Proc
Accepted Article
1964;39:427-51.
Löffel NB, Rossi LN, Mumenthaler M, et al. The Landry-Guillain-
66 barré syndrome. Complications, prognosis and natural history in 123 133
cases. J Neurol Sci 1977;33:71-9.
Hartung HP, Reiners K, Schmidt B, et al. Serum interleukin-2
concentrations in Guillain-Barré syndrome and chronic idiopathic
67a demyelinating polyradiculoneuropathy: comparison with other 131
neurological diseases of presumed immunopathogenesis. Ann Neurol
1991;30:48-53.
Hughes RA, Swan AV, Raphaël JC, et al. Immunotherapy for
67b Guillain-Barré syndrome: a systematic review. Brain 2007;130:2245- 131
57.
Raphael JC, Chevret S, Jars-Guincestre MC. Appropriate number of
67c plasma exchanges in Guillain-Barré syndrome. Ann Neurol 131
1997;41:298-306.
Schmidt B, Toyka KV, Kiefer R, et al. Inflammatory infiltrates in
sural nerve biopsies in Guillain-Barré syndrome and chronic
67d 131
inflammatory demyelinating neuropathy. Muscle Nerve.
1996;19:474-87.
Guillain-Barré Syndrome Steroid Trial Group. Double-blind trial of
71 intravenous methylprednisolone in Guillain-Barré syndrome. Lancet 129
1993;341:586-90.
Cornblath DR, Mellits ED, Griffin JW, et al. Motor conduction
72a studies in Guillain-Barré syndrome: description and prognostic value. 128
Ann Neurol 1988;23:354-9.

Ho TW, Li CY, Cornblath DR, et al. Patterns of recovery in the

72b 128
Guillain-Barré syndromes. Neurology 1997;48:695-700.

Kennedy RH, Danielson MA, Mulder DW, et al. Guillain-Barré

72c syndrome: a 42-year epidemiologic and clinical study. Mayo Clin 128
Proc 1978;53:93-99.
Ho TW, Hsieh ST, Nachamkin I, et al. Motor nerve terminal
75a degeneration provides a potential mechanism for rapid recovery in 127
acute motor axonal neuropathy after Campylobacter infection.

This article is protected by copyright. All rights reserved.

 Neurology 1997;48:717-24.

Ilyas AA, Mithen FA, Dalakas MC, et al. Antibodies to acidic

75b glycolipids in Guillain-Barré syndrome and chronic inflammatory 127
demyelinating polyneuropathy. J Neurol Sci 1992;107:111-21.
Accepted Article
Visser LH, van der Meché FG, Meulstee J, et al. Cytomegalovirus
infection and Guillain-Barré syndrome: the clinical,
75c 127
electrophysiologic, and prognostic features. Neurology 1996;47:668-
73.
Sharief MK, McLean B, Thompson EJ. Elevated serum levels of
78 tumor necrosis factor-alpha in Guillain-Barré syndrome. Ann Neurol 123
1993;33:591-6.
Illa I, Ortiz N, Gallard E, et al. Acute axonal Guillain-Barré syndrome
79 with IgG antibodies against motor axons following parenteral 121
gangliosides. Ann Neurol 1995;38:218-24.
Goust JM, Chenais F, Carnes JE, et al. Abnormal T cell
80a subpopulations and circulating immune complexes in the Guillain- 120
Barré syndrome and multiple sclerosis. Neurology 1978;28:421-5.
Jacobs BC, Endtz H, van der Meché FG, et al. Serum anti-GQ1b IgG
80b antibodies recognize surface epitopes on Campylobacter jejuni from 120
patients with Miller Fisher syndrome. Ann Neurol 1995;37:260-4.
Saida T, Saida K, Lisak RP, et al. In vivo demyelinating activity of
82 sera from patients with Guillain-Barré syndrome. Ann Neurol 117
1982;11:69-75.
Nobile-Orazio E, Carpo M, Meucci N, et al. Guillain Barré syndrome
83 associated with high titers of anti-GM1 antibodies. J Neurol Sci 116
1992;109:200-6.
Feasby TE, Hahn AF, Brown WF, et al. Severe axonal degeneration in
84a acute Guillain-Barré syndrome: Evidence of two different 115
mechanisms? J Neurol Sci 1993;116:185-92.
Kornberg AJ, Pestronk A, Bieser K, et al. The clinical correlates of
84b 115
high-titer IgG anti-GM1 antibodies. Ann Neurol 1994;35:234-7.
Koski CL, Gratz E, Sutherland J, et al. Clinical correlation with anti-
84c peripheral-nerve myelin antibodies in Guillain-Barré syndrome. Ann 115
Neurol 1986;19:573-7.
Juurlink DN, Stukel TA, Kwong J, et al. Guillain-Barré syndrome
87 after influenza vaccination in adults: a population-based study. JAMA 114
Intern Med 2006;166:2217-21.

This article is protected by copyright. All rights reserved.

 Vucic S, Kiernan MC, Cornblath DR. Guillain-Barré syndrome: an
88 111
update. J Clin Neurosci 2009;16:733-41.
McLeod JG. Electrophysiological studies in the Guillain-Barré
89 110
syndrome. Ann Neurol 1981;9:20-7.
Accepted Article
Honavar M, Tharakan JK, Hughes RA, et al. A clinicopathological
90a study of the Guillain-Barré syndrome. Nine cases and literature 108
review. Brain. 1991;114:1245-69.
Oomes PG, Jacobs BC, Hazenberg MP, et al. Anti-GM1 IgG
90b antibodies and Campylobacter bacteria in Guillain-Barré syndrome: 108
evidence of molecular mimicry. Ann Neurol 1995;38:170-5.
Yuki N, Yoshino H, Sato S, et al. Severe acute axonal form of
90c Guillain-Barré syndrome associated with IgG anti-GD1a antibodies. 108
Muscle Nerve. 1992;15:899-903.
Zochodne DW. Autonomic involvement in Guillain-Barré syndrome:
90d 108
a review. Muscle Nerve 1994;17:1145-55.
Moulin DE, Hagen N, Feasby TE, et al. Pain in Guillain Barré
94a 107
syndrome. Neurology 1997;48:328-31.
Willison HJ. The immunobiology of Guillain-Barré syndromes. J
94b 107
Peripher Nerv Syst 2005;10:94-112.
Hirota N, Kaji R, Bostock H, et al. The physiological effect of anti-
96a GM1 antibodies on saltatory conduction and transmembrane currents 105
in single motor axons. Brain 1997;120:2159-69.
van den Berg LH, Marrink J, de Jager AE, et al. Anti-GM1 antibodies
96b in patients with Guillain-Barré syndrome. J Neurol Neurosurg 105
Psychiatry. 1992;55:8-11.
Van der Meché FG, Van Doorn PA, Meulstee J, et al. Diagnostic and
96c Classification Criteria for the Guillain-Barré Syndrome. Eur Neurol 105
2001;45:133–9
Hughes RA, Wijdicks EF, Barohn R, et al. Practice parameter:
immunotherapy for Guillain-Barré syndrome: report of the Quality
99 104
Standards Subcommittee of the American Academy of Neurology.
Neurology 2003;61:736-40.
Cornblath DR. Electrophysiology in Guillain-Barré syndrome. Ann
100 102
Neurol 1990;27:S17-20.

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 Table 2. Journals in which the top-100 cited articles were published.

Rank Journal Number of

articles
1 Annals of Neurology 39
Accepted Article
2 Neurology 13
3 Brain 10
4 Lancet 6
5 Muscle & Nerve 5
5 New England Journal of Medicine 5
7 Journal of the Neurological Sciences 4
8 Journal of Neurology, Neurosurgery, & Psychiatry 3
9 JAMA Internal Medicine 2
9 Mayo Clinic Proceedings 2
11 Annals of Internal Medicine 1
11 The American Journal of Medicine 1
11 Brain Research 1
11 European Neurology 1
11 JAMA 1
11 JAMA Neurology 1
11 Journal of Clinical Neuroscience 1
11 Journal of Neuroscience 1
11 Journal of the Peripheral Nervous System 1
11 Lancet Neurology 1
11 Medicine 1

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 Table 3. Number of articles identified as GBS citation classics according to country of

origin.

Country Number of
Accepted Article
citation classics
United States of 34
America
Japan 16
United Kingdom 16
Netherlands 14
Canada 7
Germany 5
Australia 2
France 2
Italy 1
Singapore 1
Spain 1
Switzerland 1

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 Table 4. Number of articles identified as GBS citation classics according to origin of the

corresponding author. Only institutions associated with multiple articles are listed.

Rank Department Institution Number of

Accepted Article
citation classics
1 Neurology Erasmus University (Rotterdam, 12
Netherlands)
1 Neurology Johns Hopkins School of 12
Medicine (Baltimore, USA)
3 Neurology University of Tokyo (Tokyo, 5
Japan)
4 Clinical Neurological The University of Western 4
Sciences Ontario (London, ON Canada)
5 Neurology Chiba University School of 3
Medicine (Chiba, Japan)
5 Neurology Dokkyo University (Mibu, Japan) 3
5 Neurology Julius Maximilian University 3
(Würzburg, Germany)
5 Clinical Neuroscience King’s College (London, United 3
Kingdom)
5 Neurology University of Pennsylvania 3
(Philadelphia, USA)
5 Neurology New Jersey Medical School 3
(Newark, USA)
11 Neurology Heinrich Heine University 2
(Düsseldorf , Germany)
11 Neuroimmunology King’s College (London, United 2
Kingdom)
11 Neurology University of Maryland 2
(Baltimore, USA)

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 Table 5. Number of articles identified as GBS citation classics according to authors.

Only authors associated with three or more articles are listed.

Author Number of Types of author association according

Accepted Article
citation to number of citation classics
classics
Cornblath DR 20 First (n=2), co- (n=18), corresponding (n=2)
van der Meché FG 12 First (n=2), co- (n=9), corresponding (n=3)
Griffin JW 12 First (n=2), co- (n=8), corresponding (n=4)
McKhann GM 12 First (n=2), co- (n=8), corresponding (n=4)
Hughes RA 11 First (n=4), co- (n=5), corresponding (n=6)
Asbury AK 11 First (n=2), co- (n=9), corresponding (n=2)
Ho TW 10 First (n=4), co- (n=6), corresponding (n=3)
van Doorn PA 10 First (n=1), co- (n=9), corresponding (n=1)
Yuki N 9 First (n=4), co- (n=3), corresponding (n=6)
Hartung HP 9 First (n=3), co- (n=5), corresponding (n=4)
Jacobs BC 8 First (n=3), co- (n=5), corresponding (n=3)
Li CY 8 Co- (n=8)
Willison HJ 7 First (n=2), co- (n=5), corresponding (n=2)
Toyka KV 7 Co- (n=7)
Schmitz PI 6 Co- (n=6)
Chiba A 5 First (n=3), co- (n=2)
Kusunoki S 5 First (n=2), corresponding (n=5)
Feasby TE 5 First (n=2), co- (n=3), corresponding (n=2)
Hahn AF 5 First (n=1), co- (n=4), corresponding (n=1)
Mishu B 5 First (n=1), co- (n=4), corresponding (n=1)
Gao CY 5 Co- (n=5)
Kanazawa I 5 Co- (n=5)
Meulstee J 5 Co- (n=5)
Visser LH 4 First (n=2), co- (n=2), corresponding (n=2)

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 Cook SD 4 First (n=1), co- (n=3), corresponding (n=1)
Koski CL 4 First (n=1), co- (n=3), corresponding (n=1)
Kuwabara S 4 First (n=1), co- (n=3), corresponding (n=1)
Blaser MJ 4 Co- (n=4)
Accepted Article
Koga M 4 Co- (n=4)
Rees JH 3 First (n=3), corresponding (n=2)
Citation classic which has same first and corresponding author was counted as 1.

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 Legend of Figure

Figure 1.
Accepted Article
Number of articles

Year of publication

Figure 1. Years of publication for the top-100 cited GBS articles.

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