Top 100 Most Influential Articles in the Field of Myeloid Neoplasms: A Bibliometric Study

As medicine advances, there is also an ever increasing emergence of medical and scientific knowledge. This presents an urgent need to identify the most significant research findings that will lay future clinical and theoretical foundations. Therefore, there is a growing interest in the evaluation of research so as to establish the most impactful papers within a field, their authors, and their countries of origin [1]. Bibliometric analysis is a powerful tool that allows us to do this [2]. This method is based on quantitative measures and, although its efficacy in quantifying the abstract concept of “quality” is often debated [3], its use by scientists and institutions has been gradually increasing over the last few years [4]. It has implications not only for individual researchers but also for the agencies financing those researchers and for government policymakers to reorient the allocation of funds and resources [5].

Myeloid neoplasms comprise a group of hematologic malignancies that originate from a myeloid cell lineage [6]. Our understanding of the biology of myeloid neoplasms has undergone substantial changes over the last 2 centuries. Their complex pathogenesis, profound genetic heterogeneity, diagnostic dilemma, and extreme variability in response to treatment continue to challenge researchers even today [7]. The classification of these neoplasms alone has been a momentous task requiring the consensus of over a hundred pathologists, hematologists, oncologists, and geneticists [8]. The World Health Organization (WHO) releases updated and revised classification schemes for myeloid malignancies every few years as new research unravels further information about their biology. There have been quite a number of bibliometric studies done on various specialties and subspecialties [9‒16]. However, no bibliometric analysis has been performed for myeloid neoplasms. Realizing this deficiency and in an effort to bridge this gap, we performed a bibliometric analysis to identify the characteristics of the top cited articles in this field.

In September 2017, the Scopus database was searched independently by 2 reviewers (A.R. and U.I.) for citations of published articles on “myeloid neoplasms.” Keywords were extracted from a number of sources including Google, the MeSH database, the International Classification of Disease-10 (ICD-10), and the 2008 WHO classification scheme for myeloid neoplasms. In order to include a large variety of articles, no exclusion criteria were set for human versus nonhuman subjects, abstract availability, or study design. Furthermore, no restriction of time limit was imposed, and all of the journals available on the database were included. The first search comprised both original and review articles and was then modified by placing a filter available on Scopus to only include the original articles.

Our keywords consisted of “Myeloproliferative disorder,” “Polycythemia Vera,” “Acute Myeloid Leukemia,” “Chronic Myelogenous Leukemia,” “Myelofibrosis”, “Essential Thrombocythemia,” “Chronic Myelomonocytic Leukemia,” “Juvenile Myelomonocytic Leukemia,” “Atypical Chronic Myeloid Leukemia,” “Systemic Mastocytosis,” “Systemic Mast Cell Disease,” “Chronic Myeloid Leukemia,” “Acute Erythroblastic Leukemia,” “Chronic Neutrophilic Leukemia,” “Chronic Eosinophilic Leukemia,” “Polycythemia Rubra Vera,” “Myeloproliferative Neoplasms,” “Hereditary Erythrocytosis,” “Hereditary Thrombocytosis,” “Familial Myeloproliferative Neoplasms,” “Myelodysplastic Syndromes,” “Hypereosinophilic Syndrome,” “Mast Cell Disease,” “MPN,” “MDS,” “AML,” and “CML.” Each keyword was searched for in article titles, abstracts, and keywords. Articles concerning the epidemiology, diagnosis, treatment, prognosis, and molecular genetics of myeloid neoplasms were all included in the list. Scopus results were sorted by the “Cited by” filter and a list of articles was extracted. Abstracts of all the articles on the list were reviewed in order to gauge their relevance and a final list of the top 100 articles was prepared independently by the 2 reviewers, an approach introduced by Lim et al. [9]. For any article to be included in the final list, a mutual consensus between 2 reviewers was required. An analysis of citations was obtained both by Scopus and manual screening and the following information was retrieved for each article: citation count, country of origin, journal name with impact factor, year of publication, and number of authors along with their H index. For articles with authors from multiple countries, the first author’s country was regarded as the country of origin. Impact factor for journals were obtained from Thomson Reuters Journal Citation Report. Means, medians, and interquartile ranges (IQR) were calculated for both the total number of citations and the number of citations per year. Tables and charts were created using Microsoft Word and Microsoft Excel, respectively. In order to determine the correlation between the journal impact factor and the number of papers published in that journal, a Pearson product moment correlation test was applied using IBM SPSS Statistics 23.0. p < 0.05 was considered statistically significant. No ethical approval was sought for this study since it did not involve human subjects or data and was merely an evaluation of previously published data.

Table 1 lists the top 100 most cited articles in the field of myeloid neoplasms, along with their total citations and citations per year. The citations of these top 100 articles ranged from 636 to 4,039, with a median of 972.5 citations per article (IQR 578.25). The sum of all of the citations was 125,691, among which 8% were self-citations. Citations per year ranged from 15.9 to 292.5. The mean and median number of citations per year was 91.3 and 80.8, respectively (IQR 80.5).

Figure 1 represents the total citations of the articles each year. A steady number of citations was observed until 1980, after which a gradual increase was seen up to 2000. The number of citations increased rapidly thereafter, peaking in 2015 with the most number of citations (n = 8,120), followed by a steep decline. Figure 2 shows the distribution of the number of publications of the top 100 articles by 5-year intervals. The 100 most cited articles were published over a span of 47 years from 1966 to 2013, with the highest number of articles published in the 5-year period from 2001 to 2005.

The top 100 articles originated from 28 different countries. The highest number of articles (n = 69) originated from the USA, followed by Germany (n = 24), the UK (n = 24), and France (n = 17). Four publications on the list had an unidentified country of origin (Fig. 3). A total of 156 authors contributed to the 100 articles on our list, with all of them having coauthored at least 2 articles. The number of authors per paper ranged from 1 to 141, with a median number of 13 authors per article. The greatest number of articles were coauthored by H. Kantarjian (n = 12), along with other major contributors, i.e., A. Hochhaus (n = 11) and J.M. Bennet (n = 10). Table 2 lists the top authors in the field of myeloid neoplasms, along with their H indices and institutional affiliations. As depicted in Table 3, the Dana-Farber Cancer Institute (n = 18) and the University of Texas MD Anderson Cancer Center (n = 18) were affiliated with the greatest number of articles on the list, followed by Harvard Medical School (n = 11), Novartis International AG (n = 11), and the University of Chicago (n = 11).

The New England Journal of Medicine was the journal with the highest number of articles published, followed by Blood and Nature. The impact factor of the journals ranged from 2.13 to 72.40. We found a significant correlation between the impact factor of the journal and the number of articles published in that journal. Furthermore, Table 4 categorizes the articles published in each journal according to their main focus. The greatest number of articles concerning CML were published in the New England Journal of Medicine (n = 10), while those concerning AML were published equally in the New England Journal of Medicine (n = 8) and Blood (n = 8).

The 100 most frequently cited articles relevant to myeloid neoplasms identified by our bibliometric analysis are listed in Table 1. These 100 articles represent the fundamental core of research in this area and have helped shape the understanding of these disorders. Through this analysis, we obtained the overall citation activity and distribution for these 100 cited articles, which can aid in providing better discernment about the concentration, distribution, and development of research trends in this particular area of interest.

Figure 2 highlights that the articles on our 100 most-cited list were published over a span of many years, i.e., from 1966 to 2015. However, the greatest number of articles (n = 65) were published between 2001 and 2015, reflecting the dramatic upsurge of research activity in myeloid leukemias that accompanied the introduction of genomic and proteomic approaches to analysis as well as the development of novel targeted therapies. This is in contrast with bibliometric studies of other well-established fields of medicine like general surgery [10], orthopedics [11], and neurosurgery [12] that published most of their citation classics before the 1980s. However, some other fields show a similar pattern of publications like cardiovascular magnetic resonance [12] and diabetes mellitus [13]. The obliteration-by-incorporation phenomenon [17] may also be in play, suggesting that some landmark articles may not be cited as frequently anymore because the information that they have provided has become so widely incorporated into the medical field that researchers do not feel the need to cite such studies. Hence, this phenomenon often contributes to the recent peak time periods in bibliometric studies. A slight decline was observed in the publication number from 2011 to 2015. This may be explained by the fact that some elapsed time is needed for the publications to gather citations and significant reportage. Moreover, inherent bias of bibliometrics towards recent papers may lead to exclusion of some important research papers [18]. Another bibliometric analysis in the future will be able to better scrutinize this particular trend in research pertaining to myeloid neoplasms. There are no articles published before 1966, highlighting that old articles have limited significance as research advances to new peaks in this recent era.

The citation count is known to be an effective indicator of the overall impact of an article; however, it fails to highlight the article’s current influence. In order to know how important an article is at the moment, we included the “citations per year’’ in Table 1 as well. The article titled, “Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell” had the greatest number of citations and citations per year.

Table 4 showcases the journals that published the majority of the top 100 cited articles. These journals may be deemed as forming a part of the “zone 1” journals as stated by Bradford’s law [19]. This law affirms that zone 1 journals in any given field are those that are the most heavily read and cited within that field. If authors deviate from these core journals, the impact of their article in their area of focus may be reduced. More than half of the top 100 cited articles (n = 53) were published in 2 major journals, i.e., the New England Journal of Medicine and Blood. The New England Journal of Medicine is a very high impact journal that caters to a wide array of audiences, whereas Blood, despite its high profile, is a specialty-specific journal relevant to the field of hematology. This shows that research being done on myeloid neoplasms aims to encompass and reach out to a broad audience, both within this particular field of medicine and generally. As depicted by other studies as well [14‒16], we saw that there is an increasing trend towards publishing high-impact articles in specialty journals compared to other high-impact journals. In addition, there is a lack of significant correlation between the number of 100 most cited articles and the impact factor of a journal, reinforcing that high-quality, influential research will earn citations independently of the journal that it is published in.

Our analysis revealed that the greatest number of articles on the list (n = 69) originated from the USA, probably owing to the funding support provided by the NIH and other private sectors, promoting research. This lines up with findings of previous studies [10, 11]. Several European countries like Germany, the UK, and France followed, but the contribution from Asian countries was minimal.

Authors, worldwide, expect and need their individual work to be recognized and supported. This helps boost their academic and scientific work and acts to propel career advancement. Prominent authors who have their work acknowledged by the scientific community are often promoted early and held in high esteem. Research bodies are more likely to accept their work and may also ask them to act as reviewers [20]. Our study indicated that 26 authors had 5 or more publications on the 100-most-cited list, and hence, were the main forerunners in myeloid neoplasms research. In comparison, a bibliometric analysis done in the field of thrombolytic therapy identified 17 authors who had 5 or more articles on the top 100 list [21]. However, citation classics from other well-established fields have shown fewer numbers of influential authors [22, 23], suggesting that compared to these fields there is greater diversity of thought leaders in myeloid leukemia research.

Like other bibliometric analyses published, there are potential limitations to our study as well. Firstly, it has been reported that Scopus tends to miss older citations, which can lead to deletion of articles published in the pre-1980s era from our assembled list [24, 25]. Secondly, 8% of the total citations were actually author self-citations. This is higher than the average self-citation percentage (i.e., 6.5%) in general medicine [26]. This is an indication that journal citations maybe skewed owing to author self-citations or a large number of people questioning badly researched findings. This was expected, noting that many of our authors had collaborated on many studies. Thirdly, the citation frequency may showcase the impact of an article but it does not tell us about the quality of a study. For this purpose, citation analysis combined with more qualitative methods would be suitable to get a more all-inclusive idea of the significance of an article [27]. Fourthly, some of the recently published, impactful articles, despite holding future significant implications, may not have made it to the top 100 most-cited list as it takes time to garner citations [19]. Lastly, only one database (i.e., Scopus) was used in this analysis, which could have resulted in the loss of those articles not recorded in Scopus. Furthermore, citation counts and H indices may also vary from those derived from other competing databases. Despite these limitations, our study provides valuable insight into the most frequently read and cited articles relating to myeloid neoplasms.

In summary, this bibliometric analysis identified the 100 top-cited articles pertaining to myeloid neoplasms and characterized the trends in research. These articles have been carefully selected from medical literature through objective metrics and will service both researchers and clinicians. An appraisal of the top-cited articles identifies the place toward which the field is steering, the emerging avenues in research, and which areas still need more research attention so that the funding agencies can direct their resources accordingly.

The authors declare no conflict of interests.