Citation classics in central nervous system inflammatory demyelinating disease

Abstract Objectives To identify and analyze the characteristics of the most influential articles about central nervous system (CNS) inflammatory demyelinating disease. Materials and Methods The Institute for Scientific Information (ISI) Web of Science database and the 2014 Journal Citation Reports Science Edition were used to retrieve the top 100 cited articles on CNS inflammatory demyelinating disease. The citation numbers, journals, years of publication, authorships, article types, subjects and main issues were analyzed. For neuromyelitis optica (NMO), articles that were cited more than 100 times were regarded as a citation classic and described separately. Results The top 100 cited articles were published between 1972 and 2011 in 13 journals. The highest number of articles (n = 24) was published in Brain, followed by The New England Journal of Medicine (n = 21). The average number of citations was 664 (range 330–3,897), and 64% of the articles were from the United States and the United Kingdom. The majority of the top 100 cited articles were related to multiple sclerosis (n = 87), and only a few articles reported on other topics such as NMO (n = 9), acute disseminated encephalomyelitis (n = 2) and optic neuritis (n = 2). Among the top 100 cited articles, 77% were original articles. Forty‐one citation classics were found for NMO. Conclusions Our study provides a historical perspective on the research progress on CNS inflammatory demyelinating disease and may serve as a guide for important advances and trends in the field for associated researchers.


| INTRODUCTION
Central nervous system inflammatory demyelinating disease (CIDD) is a term that encompasses a broad spectrum of diseases such as multiple sclerosis (MS), neuromyelitis optica (NMO), acute disseminated encephalomyelitis (ADEM), optic neuritis (ON), and transverse myelitis. MS is a prototypic form of CIDD that has garnered great interest by researchers worldwide due to its high prevalence, young age of onset and chronicity, which results in a significant social burden (Adelman, Rane, & Villa, 2013). Recent understanding of the role of aquaporin-4 (AQP4) antibodies in NMO has enhanced researcher attention in this field . As a result, numerous papers were published regarding these diseases, and the clinical characteristics and treatment strategies were decided to some degree (Aleixandre-Benavent et al., 2015; Wingerchuk & Carter, 2014). However, there is increased demand to stratify the current literature regarding idiopathic inflammatory demyelinating disease to serve as a guide to researchers.
Bibliometrics is a research method that analyzes citation frequencies and patterns of articles in a category of interest (Moed, 2009).
Although there is some debate as to the association between the number of citations and the quality of the study, highly cited articles can indirectly represent the impact of a particular article on the scientific community and the trends in a specific field of research (Moed, 2009). The results of a citation analysis can suggest "classic lists" of articles in a specific field and "hints" about trends in citations within an area.

| MATERIALS AND METHODS
The Web of Knowledge Journal Citation Reports Science Edition 2014 (Thomson Reuters, New York, NY, USA) was used to search for all journals that are listed under the categories "clinical neurology", "neuroscience" and "medicine, general & internal". We retrieved all articles that were cited more than 100 times in the selected jour- To find the CIDD-related works among all the articles that had been cited more than 100 times in the three categories, we used following search terms: "multiple sclerosis", "demyelinating disease", "myelitis", "optic neuritis", "clinically isolated syndrome", "neuromyelitis optica", "Devic's disease", "Balo concentric sclerosis", "Schilder's diffuse sclerosis", "Schilder's disease", "diffuse myelinoclastic sclerosis", "Marburg multiple sclerosis", "acute disseminated encephalomyelitis", "solitary sclerosis", "acute hemorrhagic leukoencephalitis", "neuromyelitis optica-immunoglobulin G (NMO-IgG)", and "aquaporin-4 antibody". The search terms for the citation classics on NMO included "neuromyelitis optica", "Devic's disease", "NMO-IgG", and "aquaporin-4 antibody". The original texts of all the searched articles were evaluated for their applicability. The citation classics on NMO were defined as articles that were cited more than 100 times (Garfield). The lists of the 100 top cited articles on CIDD and the citation classics on NMO were obtained and analyzed for their characteristics: number of citations, year of publication, published journal, authorship, country and institution of origin, type of article, subject of article (e.g., MS, NMO, ADEM, ON, etc.) and main issues. The country and institution of origin was defined by the affiliation of the first author. If the first author had more than one affiliation, the affiliation of corresponding author was used. Two researchers independently reviewed the data (J.E.K and K.M.P) and any disagreements were decided by further discussion with another neurologist (J.S.B). This study did not need to be reviewed by an ethics committee since it performed a bibliometric analysis of existing published studies.

| Characteristics of the top 100 cited articles of CIDD
The list of the top 100 cited articles on CIDD are presented in Table 1.
The average number of citations for the top 100 cited articles were 664 (range, 330-3,897). The articles were published between 1972 and 2011, and the majority of the articles were published after 1995 ( Figure 1a). There were 64 articles that were cited more than 400 times, which is the criteria commonly used as the threshold for a citation classic (Garfield) Table 2). The highly cited articles were published in 13 journals, which was led by Brain (n = 24) and closely followed by The New England Journal of Medicine (n = 21) (Table S1).
Fifty-three authors were found to have contributed more than three articles on the list. Miller DH was the most prolific author for the 100 articles, followed by Weinshenker BG and Polman CH (Table S2) A considerable portion of the papers also discussed the pathological findings of CIDD (n = 16).

| Citation classics of NMO
Using the cut-off threshold of 100 citations, we found 41 citation classics for NMO (   Table 4] and was subsequently followed by the suggestion of revised diagnostic criteria that included NMO-IgG positivity in the diagnosis [rank 1 in Table 4]. These two articles had a significant role in discriminating NMO from MS. There are eight different countries of origin for the citation classics (Table 2). USA (n = 20) had the largest number of articles, which was followed by the UK (n = 6), Japan (n = 5) and Germany (n = 4). The Mayo Clinic (Minnesota, USA) was the most active publishing institution for the NMO citation classics ( Table 2). The citation classics were published in 13 journals, which was led by Neurology (n = 15), followed by Brain (n = 7), Archives of Neurology (n = 5) and Annals of Neurology (n = 3; Table S1). Twenty-four authors contributed 3 or more of the articles on the citation classics list. Weinshenker BG had the highest number of articles, followed by Wingerchuk DM, Pittock SJ, Lennon VA, and Lucchinetti CF (Table S3). Among the 41 articles, 5 were review articles or guidelines [ranks 1,4,28,29,40 in Table 4], 1 was a case report [rank 37 in Table 4], and the remainder of the articles was original research articles. Four articles reported basic science studies [ranks 14,16,17,20 in Table 4]. The main issues discussed in the citation classics for NMO and their trends over time are summarized in Table 3 and Figure 2b. The most frequently discussed topic among the citation classics was the serological markers, NMO-IgG or AQP4 anti-  Table 4]. Other frequently cited issues included NMO pathology [ranks 5,7,13 in Table 4], the effect of various treatments (rituximab or prednisolone with azathioprine) [ranks 8,18,19 in Table 4], and MRI characteristics [ranks 6,9,38 in Table 4].

| DISCUSSION
In the current study, we identified and characterized the top 100 cited articles concerning CIDD. Using this bibliometric approach, we can examine the historical progress within a field of interest and inform researchers of the articles or authors that have had a significant impact on the field. this unique phenotype (Kuroiwa & Shibasaki, 1976 Guideline/review/meta-analysis 5 Basic research 4 CNS, central nervous system. T A B L E 2 (Continued) T A B L E 2 Countries and institutions of origin for the citation classics in the field of central nervous system inflammatory demyelinating disease (a) and neuromyelitis optica (b)

Countries of origin
USA 41 UK 23 The Netherlands 9 Italy 6 Germany 5 . This study had a different viewpoint and methodological approach from our study, which might explain the discordance between the results of the two studies.
We analyzed the top 100 cited articles on CIDD published during an Our research has some limitations that should be considered. First, as aforementioned, temporal bias is inevitable in a bibliometric analysis. Older articles can be more or less cited due to increased opportunities to be cited over time and the "obliteration by incorporation" phenomenon (Bohannon & Roberts, 1991;Garfield, 1987). There Here, we presented a detailed list of the top 100 cited articles for the topic CIDD and also separately propose citation classics for NMO using bibliometric methods. A strength of our research is that we included all types of articles published worldwide during an unrestricted time period. Although the citation rate does not directly represent the quality of the study, it is one marker used to recognize the importance of studies in the scientific community. We can trace scientific progress and identify seminal articles in a specific field by citation analysis.