Tumor Biol. DOI 10.1007/s13277-014-1608-7

RESEARCH ARTICLE

An analysis of the most-cited research papers on oncology: which journals have they been published in? Faruk Tas

Received: 25 November 2013 / Accepted: 2 January 2014 # International Society of Oncology and BioMarkers (ISOBM) 2014

Abstract The most-cited papers (MCPs) are likely those that impressed researchers and had profound influence on clinical practice or future developments in the related scientific field. This study was conducted to explore a bibliometric approach to assess where the oncology-related MCPs have been published in. The source of the data presented in this study was provided by using the InCitesTM, Web of Science, Thomson Reuters Database (2013). It contained any journal indexed by ISI between 1979 and 2013. The term MCPs arbitrarily defined as equal or more than 100 citations. A total of 565 publications were cited equal or more than 100 times. They were published in 79 different journals (64 oncology, 12 medicine, and 3 science), led by the Journal of Clinical Oncology (n=76; 13.5 %) and Cancer Research (n=66; 11.7 %) followed by Oncogene (n= 46; 8.1 %), Nature Reviews Cancer (n=41; 7.3 %), and Cancer (n=37; 6.5 %). Moreover, the journal categories with the MCPs were the Oncology with 495 articles (87.6 %), followed by the Medicine with 60 (10.6 %) articles. However, the numbers of journals related to Science (n=10; 1.8 %) were the least. The MCPs were cited a total of 118,531 times. The citations ranged from 100 to 1,790, and the median number was 149. The total numbers of MCPs were the most prominent for the journals, the New England Journal of Medicine (median 398), Lancet (median 213), and Nature Reviews Cancer (median 210). In other side, the counts of MCPs were the highest for the Science and Medicine-categorized journals (median 212.5 and 192.5 citations, respectively). The MCPs categorized as Oncology were the least cited (median 145). The median number of MCPs per year was 18.7 with range 4.1–858.5. F. Tas (*) Institute of Oncology, University of Istanbul, Capa, 34390 Istanbul, Turkey e-mail: [email protected]

The annual most valuable MCPs were also published in the journal Nature Reviews Cancer (median 42) and the New England Journal of Medicine (median 38.7). Likewise, the numbers of MCPs were the highest for the Sciencecategorized journals (median 37), whereas the citations per year were significantly lower in Medicine and Oncology-categorized journals (25.8 and 17.8, respectively). In conclusion, most of the MCPs were published in Oncology specialized journals. Keywords Oncology . Web of science . Most-cited papers

Introduction It is generally accepted that number of publication represents the main part of a research process and the best indicator of the scientific performance [1–3]. The citation rating, another important indicator, is a popular method for evaluating the impact of an investigator or a publication in the scientific community. Recently, it is widely accepted that citation rating is one of the best methods currently available for measuring the merit of a paper and a journal. Besides, the frequency of citing has significant implications for institutions and even nations in addition to journals and authors. Therefore, a remarkable citation history of a paper or journal often signifies great reputation in a particular area of research. The most-cited papers (MCPs) are likely those that impressed researchers and had profound influence on clinical practice or future developments in the related scientific field [2, 4]. So far, various specialties have attempted to show MCPs in their fields [2–8]. However, no study was published in this issue for field of oncology. In order to review the MCPs dedicated to oncology, we conducted the current study to focus exclusively on the MCPs in an attempt to provide a bibliometric perspective of oncology-related researches. We

Tumor Biol.

only intended to identify the journals where the MCPs have been published in.

Material and methods The source of the data presented in this study was provided by using the InCitesTM, Web of Science, and Thomson Reuters Database (2013). We identified journals for publications in “Subject Area” section by using “ONCOLOGY” in the column. This provided a list of all articles appearing in a given journal ranked by citation count. Articles were ranked according to how many times they were cited by any journal indexed by ISI between 1979 and 2013. The database for this study was compiled in August 13, 2013, and the numbers presented thus reflect the citation counts at that time (data processed in May 24, 2013). For this analysis, a sample size of at least 100 original contributions in each of the articles was regarded as MCPs. Besides, each journal was categorized into one of the medical/ science disciplines such as Science, Medicine, and Oncology.

citations per year were significantly lower in Medicine and Oncology-categorized journals (25.8 and 17.8, respectively). In the oncology-related MCPs published from 1981 to 2011, the years 2005 and 2007 were the years with the greatest number of MCPs (n=57 and n=55, respectively), followed by

Table 1 The MCP counts in descending order of the number of citations they received according to journal and journal categories Classification Journals of journal

n

Oncology

495 76 66 46 41

Journal of Clinical Oncology Cancer Research Oncogene Nature Reviews Cancer Cancer Journal of The National Cancer Institute Clinical Cancer Research Cancer Cell British Journal of Cancer Cancer Epidemiology Biomarkers & Prevention Carcinogenesis International Journal of Cancer Seminars in Oncology European Journal of Cancer Annals of Oncology International Journal of Radiation Oncology Biology Physics Biochimica Et Biophysica Acta-Reviews on Cancer Cancer Letters Lancet Oncology Leukemia Radiotherapy and Oncology Advances in Cancer Research Anticancer Research Ca: a Cancer Journal for Clinicians Cancer and Metastasis Reviews Cancer Treatment Reviews Critical Reviews in Oncology Hematology Endocrine-Related Cancer Gynecologic Oncology Journal of Thoracic Oncology Seminars in Cancer Biology Others* (n=33)

Results A total of 30,106 papers were identified in the search. Among them, 565 (1.9 %) publications were identified that met the aforementioned criteria; cited equal or more than 100 times. The 565 MCPs were published in 79 different journals (64 oncology, 12 medicine, and 3 science), led by the Journal of Clinical Oncology (n=76; 13.5 %) and Cancer Research (n=66; 11.7 %) followed by Oncogene (n=46; 8.1 %), Nature Reviews Cancer (n= 41; 7.3 %), and Cancer (n=37; 6.5 %) (Table 1). Moreover, the journal categories with the MCPs were the Oncology with 495 articles (87.6 %), followed by the Medicine with 60 (10.6 %) articles. However, the numbers of journals related to Science (n=10; 1.8 %) were the least. Our 565 eligible MCPs were cited a total of 118,531 times. They had 28.1 % of all 421,757 citation counts. The citations ranged from 100 to 1,790, and the median number was 149 (Table 2). The total numbers of MCPs were the most prominent for the journals, the New England Journal of Medicine (median 398), Lancet (median 213), and Nature Reviews Cancer (median 210). In other side, the counts of MCPs were the highest for the Science and Medicine-categorized journals (median 212.5 and 192.5 citations, respectively). The MCPs categorized as Oncology were the least cited (median 145). The median number of MCPs per year was 18.7 with range 4.1 to 858.5 (Table 3). The annual most valuable MCPs were also published in the journal Nature Reviews Cancer (median 42) and the New England Journal of Medicine (median 38.7). Likewise, the numbers of MCPs were the highest for the Science-categorized journals (median 37), whereas the

Medicine Lancet New England Journal of Medicine JAMA-Journal of the American Medical Association Journal of Pathology Stem Cells

37 25 22 14 11 11 11 11 8 7 6 6 5 5 5 5 5 4 3 3 3 3 3 3 3 3 3 41 60 16 13 8 6 6

Tumor Biol. Table 1 (continued)

Table 3 The journals and journal categorizes regarding citation counts per year on oncology

Classification Journals of journal

n Median (range)

Others** (n=7) Science Proceedings of the National Academy of Sciences of the United States of America Nature Science Total

11 10 4 3 3 565

*Annals of Surgical Oncology (2), Breast Cancer Research (2), Breast Cancer Research and Treatment (2), Cancer Causes & Control (2), Molecular Cancer Therapeutics (2), Nutrition and Cancer-An International Journal (2), Oncologist (2), Pediatric Blood & Cancer (2), BMC Cancer (1), Cancer Biology & Therapy (1), Cancer Chemotherapy and Pharmacology (1), Cancer Cytopathology (1), Cancer Genetics and Cytogenetics (1), Cancer Investigation (1), Cancer Surveys (1), Chemotherapy (1); Critical Reviews In Oncogenesis (1), European Journal of Cancer Prevention (1), Genes Chromosomes & Cancer (1), International Journal of Oncology (1), Journal of Neuro-Oncology (1), Journal of Pediatric Hematology Oncology (1), Journal of The National Comprehensive Cancer Network (1), Leukemia Research (1), Lung Cancer (1), Medical Dosimetry (1), Melanoma Research (1), Molecular Cancer Research (1), Oncology (1), Oncology Reports (1); Oncology Research (1), OncologyNew York (1), Seminars in Surgical Oncology (1) **Annals of Internal Medicine (2), Cell (2), Experimental Cell Research (2), Journal of Experimental Medicine (2), Journal of Clinical Investigation (1), Journal of Environmental Science and Health (1), Nature Medicine (1)

Table 2 The journals with at least ten MCPs and journal categorizes regarding citation counts Median (range) Journal Name New England Journal of Medicine Lancet Nature Reviews Cancer Cancer Epidemiology Biomarkers & Prevention Carcinogenesis Journal of the National Cancer Institute Journal of Clinical Oncology Oncogene Cancer Research Cancer Cell Cancer Clinical Cancer Research International Journal of Cancer British Journal of Cancer Journal Group Science Medicine Oncology Total

398 (116–801) 213 (100–777) 210 (103–1,534) 174 (100–401) 157 (100–511) 155 (108–761) 153 (101–928) 148.5 (100–722) 146.5 (100–766) 146 (111–566) 138 (102–640) 135 (100–371) 133 (108–1,015) 123 (101–194) 212.5 (121–1,790) 192.5 (100–848) 145 (100–1,717) 149 (100–1,790)

Journal Name Nature Reviews Cancer New England Journal of Medicine Lancet Cancer Cell Journal of Clinical Oncology International Journal of Cancer Oncogene Cancer Epidemiology Biomarkers & Prevention Journal of the National Cancer Institute Carcinogenesis Cancer Research British Journal of Cancer Clinical Cancer Research Cancer Journal Group Science Medicine Oncology Total

42.0 (10.8–139.5) 38.7 (8.3–160.2) 26.6 (6.3–155.4) 25.3 (13.9–70.5) 23.5 (6.2–138.2) 19.8 (5.1–296.7) 17.8 (7.1–92.5) 16.6 (7.7–58.0) 15.4 (6.7–85.0) 14.3 (5.9–72.0) 13.0 (4.4–85.1) 12.6 (5.9–32.3) 12.5 (6.7–46.4) 11.5 (5.1–64.0) 37.0 (13.7–227.8) 25.8 (6.3–212.0) 17.8 (4.1–858.5) 18.7 (4.1–858.5)

2006 (n=50). Although the citation distributions showed some annual fluctuations, generally, the MCPs were increased gradually over time to 2005–2007 years, and decreased sharply to the year 2011 (Fig. 1). The citation and annual citation numbers are showed depending on time intervals in Table 4.

Discussion The world output in oncology increased on average with 4.9 % per year [9]. Many evaluative-bibliometric studies have focused on the field of oncology [9–12]. This attention reflects the importance of oncological research especially in developed countries, an overview of the productivity and impact of oncological research in the European Union. Comparing results on publication output and citation impact per country presented in these studies. The present study showed several features of MCPs in field of oncology research during the past 33 years by means of literature review. As expected, our study found that most of the MCPs were published in high-impact journals, with is consistent with the results of other trials. This supports the well-known paradigm that MCPs are often published in journals topping the impact factor list, which maintains the high-impact factor of these articles [1, 2]. The outcome that nonspecific oncology journals contain on average less papers, both totally and annually than specific

Tumor Biol. Fig. 1 Frequency distribution of the regarding oncology-related MCPs according to years

No. of MCPs 60

50

40

30

20

10

0 1975

1980

1985

1990

1995

2000

2005

2010

2015

-10

journals in the journal category oncology is rather trivial, but the finding that their impact factors tend to be higher than those for the journals in the oncology category [9]. A possible explanation for these findings is that authors who submit a paper to a more generalized journals with high-impact factor present findings that are relevant not merely to their specific community, but to a wider scientific audience. Therefore, publishing a paper in a more general journal leads to a wider reading audience than in oncological specialist journals and consequently, it generates a higher citation impact. Our study has two limitations. Our study was that the search only used the ISI Web of Knowledge database and did not include other well-known databases such as Scopus and Google Scholar. Because these databases contain more journals and have wider international journal coverage, they generally provide higher citation counts than Web of Science. Unlikely, we overcome another limitation regarding the inherent bias of the citation analysis. The total citations accumulated over time which means that older publications would definitely receive more citations than the new ones [2]. The publications with a short span of time to generate citation rates are possibly underestimated with respect to their citation number. Therefore, we eliminated this conflicting issue by using citation number per year parameter.

Table 4 Frequency distribution of the regarding oncology-related MCPs according to years Year

n

Citation number Median (range)

Citation number per year Median (range)

1979–1989 1990–2000 2001–2011

10 150 405

164.5 (103–398) 150.5 (100–1,790) 146.0 (100–1,717)

6.1 (4.1–16.6) 9.6 (4.6–94.2) 22.8 (8.7–858.5)

In conclusion, this work represents the first bibliometric assessment of different research quality in oncology-related literature. Interest in oncology as a serious clinical problem continues to grow. The published in high-impact journals are most likely to be cited in the field of oncology research. As more publications on oncology take place in non-oncology journals with high-impact factors, the awareness of oncology will probably extend to all researchers in addition to the specialists to cancer. Conflicts of interest None Source of funding No funding source

References 1. Garfield E. The history and meaning of the journal impact factor. JAMA. 2006;295:90–3. 2. Tao T, Zhao X, Lou J, Bo L, Wang F, Li J, et al. The top cited clinical research articles on sepsis: a bibliometric analysis. Crit Care. 2012;16:R110. 3. Tasli L, Kacar N, Argenziano G. A scientometric analysis of dermoscopy literature over the past 25 years. J European Acad Dermatol Venereol. 2011;26:1142–8. 4. Nieder C, Grosu A, Mehta MP. Brain metastases research 1990– 2010: pattern of citation and systematic review of highly cited articles. The Scientific World J 2012; Article ID 721598. 5. Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg. 2002;26: 1099–105. 6. Ponce FA, Lozano AM. Highly cited works in neurosurgery. Part I: the 100 top-cited papers in neurosurgical journals. J Neurosurg. 2010;112:223–32. 7. Celayir S, Sander S, Elicevik M, Vural A, Celayir AC. The most commonly cited articles in pediatric surgical journals. Eur J Pediatr Surg. 2008;18:160–3.

Tumor Biol. 8. Feijoo JF, Limeres J, Fernandez-Varela M, Ramos I, Diz P. The 100 most cited articles in dentistry. Clin Oral Invest 2013, June 15, on line published. 9. Lopez-Illescas C, Moya-Anegon F, Moed HF. The actual citation impact of European oncological research. Eur J Cancer. 2008;44: 228–36.

10. Ugolini D, Mela GS. Oncological research overview in the European Union. A 5-year survey. Eur J Cancer. 2003;39:1888–94. 11. Lewison G. The publication of cancer research papers in high impact journals. ASLIB PROC. 2003;55:379–87. 12. Tas F. The contribution of countries and world regions in productivity of oncological publication. Ann Oncol. 2008;19:1962–8.

An analysis of the most-cited research papers on oncology: which journals have they been published in?

The most-cited papers (MCPs) are likely those that impressed researchers and had profound influence on clinical practice or future developments in the...
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