Identifying Trends in Oncology Research through a Bibliographic Analysis of Cancer Research and Treatment

Article information

Cancer Res Treat. 2025;57(1):11-18

Publication date (electronic) : 2024 December 5

doi : https://doi.org/10.4143/crt.2024.688

Choong-kun Lee¹, Jeong Min Choo², Yong Chan Ahn³, Jin Kim², Sun Young Rha^,1, Chai Hong Rim^,4, On behalf of the 50th Anniversary Committee of the Korean Cancer Association

¹Division of Medical Oncology, Department Internal Medicine, Yonsei Cancer Center, Yonsei University College of Medicine, Seoul, Korea

²Division of Colorectal Surgery, Department of General Surgery, Korea University College of Medicine, Seoul, Korea

³Department of Radiation Oncology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

⁴Department of Radiation Oncology, Korea University Ansan Hospital, Korea University College of Medicine, Ansan, Korea

Correspondence: Sun Young Rha, Division of Medical Oncology, Department of Internal Medicine, Yonsei Cancer Center, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea Tel: 82-2-2228-8053 Fax: 82-2-362-5592 E-mail: rha7655@yuhs.ac

Co-correspondence: Chai Hong Rim, Department of Radiation Oncology, Korea University Ansan Hospital, Korea University College of Medicine, 123 Jeokgeum-ro, Danwon-gu, Ansan 15355, Korea Tel: 82-31-412-6850 Fax: 82-31-412-6851 E-mail: crusion3@naver.com

*Choong-kun Lee and Jeong Min Choo contributed equally to this work.

Received 2024 July 22; Accepted 2024 December 4.

Abstract

Introduction

Driven by the expanding population within the cancer-prone old age group and scientific advancements in cancer screening, diagnosis, and treatment, the importance of cancer and related diseases in public health increases [1]. Cancer is currently the leading cause of deaths in Korea and significantly affects societal health issues. Advancements in expanded screening program and treatment, however, have greatly improved prognosis of cancer, and the 5-year relative survival rate increased from 57.1% (1993-1995) to 72.1% (2017-2021) [2].

Different cancers exhibit varying disease characteristics and prognoses. Nevertheless, they usually share the fundamental principles of underlying pathophysiology, diagnosis, and treatment, such as the biological traits of hyper-division and metastatic potential, cytotoxic or targeting mechanisms of anticancer drugs, cancer-killing effects of radiation, and general principles of radical surgery [3]. With the growing complexity in cancer management, multidisciplinary strategy has been highly emphasized [4]. Hence, academic societies focused on oncology, in which oncologists majoring diverse fields can collaborate, may play a pivotal role.

The Korean Cancer Research Society (KCRS) was founded in 1958, and later was reorganized into the Korean Cancer Association (KCA) as an academic institution in 1974. The KCA (former KCRS) has steadily expanded its influence on cancer research and academic activities in Korea. The KCRS began to publish Journal of the Korean Cancer Association (JKCA) as the official journal from 1966. Though the KCRS was renamed as the KCA from 1974, the journal title of JKCA was maintained until early 2001, and it was changed in Cancer Research and Treatment (CRT) thereafter with the refreshing ambition of promoting to become Science Citation Index Expanded (SCIE) level journal. From 2002 till 2005, CRT used to be a bimonthly journal, and after 2006, it became a quaternary one. The planned number of articles per year used to be 40, which became more than double since 2015. Until before CRT’s registration to SCIE in 2012-2013, the number of manuscript submission was not big enough, with the average of 66. Since after CRT’s SCIE enlistment, the manuscript submission number has dramatically increased. Though the acceptance rate decreased significantly, the number of accepted articles increased a lot, which resulted in long waiting time (longer than 1 year) until the official publication after review completion. In order to endorse the “timely publication”, which is one of the academic journals’ important missions to propagate the newest information, the editorial board determined to increase the article publication number (more than double) per year.

In this study, quantitative and qualitative analyses were performed of the publication trends in CRT, an official journal of KCA, over the past two decades (2004-2023), which could reflect the oncology research trend and provide suggestions for future perspectives.

Materials and Methods

The numbers of manuscripts submitted to CRT and the acceptance rates from 2004 till 2023 were investigated to evaluate academic activity. To evaluate the trend of research characteristics, all articles published in CRT between 2004 and 2023 were extracted from the PubMed database. All publications except retracted ones were included in this investigation. The classification method in the current study referenced the framework outlined in “40 Years of Cancer Research through the Journal of the Korean Oncology Society” [5].

Studies in which all authors belonged to a single institution were classified as single-center studies, and those involving authors from two or more institutions were classified as multicenter studies. In the institutional classification, universities were prioritized over hospitals, and studies from multiple affiliated institutions within the same university were considered single-center studies. The main and the most representative disease entity (i.e., type of cancer) in each study was investigated and assigned.

Each article was classified based on the first author’s research field (e.g., internal medicine, general surgery, or pathology, etc.). All studies were classified into preclinical, translational, and clinical studies. Preclinical and translational studies classified into the fields such as cell biology, genetics, immunology, pathology, pharmacology, and etiology, based on the subject. Clinical study designs were further classified as follows: (1) prospective or retrospective studies based on patient recruitment; (2) randomized studies, nonrandomized controlled studies, case series, case studies, national database research, or systematic reviews based on the type of data collection and analysis; and (3) surgery, radiotherapy, systemic treatment, mixed treatment, supportive care, diagnosis, clinical features, and etiological analysis based on the study subjects, respectively. Studies addressing multiple subjects were classified based on the most representative one.

The number of publications per institution was analyzed based on the corresponding author’s institution. Studies in which the corresponding author was affiliated to a foreign institution were classified as foreign researches. To assess temporal trends, the study period (2004-2023) was segmented into 5-year intervals for analysis.

Results

1. Changing trends of numbers of submitted manuscripts, published articles, and acceptance rates

CRT has been registered in the SCIE since 2012/2013. Prior to this registration, from 2004 till 2012, the average number of submitted manuscripts was 65.7±18 per year. In contrast, it increased to 791±371.4 per year from 2013 to 2023 (Fig. 1). There was more than a tenfold increase since after CRT’s SCIE registration when compared with the previous era, and more than 1,000 manuscripts were submitted since after 2020.

Fig. 1.

Number of submissions and acceptance rate. CRT, Cancer Research Treatment.

The number of published articles annually used to be 64 in 2004, which gradually declined to 32 until 2007. It was approximately 40 articles from 2008 till 2013, and then rapidly increased to 117 in 2015 (Fig. 2). From 2004 till 2014, 32-64 articles (average 45.2±9.9 articles) were published annually, which increased to 117-162 articles (average 132.3±17.8 articles) annually since after 2015 till 2023.

Fig. 2.

Number of publications per year. SCIE, Science Citation Index Expanded.

Reviewing data from before the 2000s, the number of publications increased significantly from the 1970s to the 1990s, averaging 100 articles per year [5]. Since 2000, many research institutions have emphasized objective indices such as SCIE, which contributed to a decrease in submissions to CRT [6]. Following CRT’s registration in SCIE, the number of submissions increased dramatically, however, the number of publication was not increased during the first few years. This resulted in an average waiting time of longer than 1 year, and in order to endorse timely publication, the editorial board determined to double the annual publication number in April 2015 for the time being.

There was a notable change in the acceptance rates before and after CRT’s SCIE registration. The average acceptance rate was 68.9%±12.9% from 2004 till 2012, which decreased to 19.3%±10.0% from 2013 to 2023. Overseas submissions were minimal (fewer than 10 annually) before 2012, but increased substantially thereafter, reaching between 826 and 1,066 submissions per year over the recent 4 years (2020-2023) (Fig. 1).

2. Changing trends of characteristics of published articles: main disease subject and study natures

Many studies focused on common Korean diseases such as stomach, breast, lung, colon, and gynecological cancers. These corresponded to the top three cancers with the highest incidence among men (stomach, lung, and colon) and women (breast, colon, and stomach) in Korea [2]. Although thyroid cancer is one of the most common cancers among women, article on thyroid cancer was rarely published. On the contrary, though hematologic malignancy was relatively rare disease and not included among the top ten most frequent cancers [2], it has been actively researched accounting for 5%-7% of all studies. From 2004 to 2013, the largest number of studies were on stomach cancer, however, from 2014 to 2023, breast cancer and lung cancer became the most common disease subjects (Fig. 3). According to Korean statistics, this trend corresponded to a decreasing incidence of stomach cancer and an increasing trend of breast cancer [2].

Fig. 3.

Main disease subject distribution of publications. CNS, central nervous system; CRC, colorectal cancer; GU, genitourinary; GY, gynecology; HN, head and neck; PB, pancreato-biliary.

Multicenter studies accounted for 24.5% and 19.6% during 2004-2008 and 2009-2013, which increased to 52.8% and 53.9% during 2014-2018 and 2019-2023 (Fig. 4). This dramatic change seems to have been influenced by CRT’s SCIE registration in 2012/2013.

Fig. 4.

Number of publications from single-center or multicenter studies.

Across all data surveyed in this study, internal medicine, including medical oncology, accounted for the largest share (35%-52%), followed by radiation oncology (9%-18%), surgery (3%-11%), and pathology (4%-8%), respectively. From 2014 to 2023, after SCIE registration, the proportion of studies on internal medicine increased from 42%-52%, when compared to that in 2004-2013 (35%-36%) (Fig. 5).

Fig. 5.

Research field (first authors) of publications. GS, general surgery; GU, genitourinary; GY, gynecology; HN, head and neck surgery; IM, internal medicine; Lab, laboratory research; Path, pathology; Ped, pediatric; PM, preventive medicine; RO, radiation oncology.

Clinical studies accounted for the largest proportion (62.2%-81.7%) across all the years surveyed. Preclinical or translational studies accounted for 38.8% of the research from 2004 to 2008, however, it decreased to approximately 20.3% from 2019 to 2023 (Fig. 6). The number of clinical studies increased from 145 between 2004 and 2008 by approximately 3.6 times, to 519 between 2019 and 2023, whereas the number of preclinical or translational studies increased by approximately 1.5 times from 88 to 132 during the corresponding periods.

Fig. 6.

Number of clinical, preclinical, and translational study publications.

Although both retrospective and prospective studies have generally increased in recent years, the number and proportion of prospective studies have significantly increased (Fig. 7). The proportions of prospective study used to be 26.3% (35/133) from 2004 till 2008, and 7.9% (12/152) from 2009 till 2013. This increased to 18.3% (95/518) from 2014 to 2018, and further 28.4% (139/490) from 2019 till 2023.

Fig. 7.

Temporal design of clinical studies. Numbers in the graphs are publication counts.

The most common clinical research method was case series throughout the study period (Fig. 8). Case reports used to comprise a significant portion in the past, but recently decreased. Between 2004 and 2008, case reports accounted for 15.8% (21 papers), whereas they accounted for 29.6% (45 papers) between 2009 and 2013. Subsequently, the proportion decreased significantly to 8.5% (44 papers) from 2014 to 2018, and further decreased to 2.9% (14 papers) between 2019 and 2023. Randomized studies comprised a small proportion across the periods of surveillance. However, although very few number of randomized studies were published before 2013, 28 studies (5.7%) were published in the most recent period between 2019 and 2023. Although no systematic literature analyses were published before 2013, 12 and 11 papers were published between 2014 and 2018 and between 2018 and 2023, accounting for 2.3% and 2.2%, respectively. The proportion of database studies that primarily utilized cancer statistics has also increased, with 102 studies (20.8%) in the most recent period between 2019 and 2023.

Fig. 8.

Study design of clinical studies. Numbers in the graphs are publication counts. NRCT, nonrandomized controlled trials; RCT, randomized controlled trials.

The study subjects of clinical research include systemic treatments, combined treatments, radiotherapy, and clinical features. Previously, studies on diagnosis comprised only 1.9%-4.6%, which, however, increased to 21.4% (105 studies) in the most recent period (2019-2023) (Fig. 9).

Fig. 9.

The distribution of study subjects examined in clinical studies.

Overall, cell, genetic, and pathology studies have been the mainstay among preclinical and translational studies (Fig. 10). When comparing the periods before and after 2013, publication on genetic research increased significantly, whereas that on pathology research decreased. From 2004 to 2008, genetic research comprised 12 of 77 studies (15.6%), which increased to 10 of 44 studies (22.7%) between 2009 and 2013. From 2014 to 2018, it further increased to 41 out of 107 (38.3%), and from 2019 to 2023, it reached 64 out of 130 (49.2%) studies. In contrast, pathology research constituted 35.1% of all studies between 2004 and 2008 and 36.4% between 2009 and 2013. However, this trend decreased in the following years, dropping to 3.7% between 2014 and 2018, and 13.8% between 2019 and 2023.

Fig. 10.

The distribution of study subjects examined in preclinical studies.

According to the corresponding authors’ affiliation, The Catholic University of Korea, Seoul National University, National Cancer Center, Yonsei University, University of Ulsan, and Sungkyunkwan University were the most prolific institutions in publishing research (Table 1). Before 2013, studies submitted from countries other than South Korea were rare, which, however, increased significantly after 2014. Overseas research publications accounted for 16.3% of the total publication between 2014 and 2018, and 22.7% between 2019 and 2023. Among the identified foreign institutions, China contributed the most, followed by the United States and Japan. Sun Yat-sen University published a significant number of research papers in CRT, which rivals major domestic institutions, with 15 papers published between 2014 and 2018 and 22 papers published between 2019 and 2023.

Table 1.

Publications sorted by corresponding authors’ affiliations

Discussion

Although approximately 150 papers were published in CRT throughout the 1980s, the journal achieved significant development in the 1990s with over 1,000 publications [5]. Subsequently, the importance of international indices such as the SCIE, has been emphasized in the academic field. However, since CRT had not yet been registered for SCIE, the number of publications was relatively small (32-64 per year from 2004 to 2013). After SCIE registration, number of submissions from overseas as well as from domestic authors has been significantly increased, and 117-162 articles were published annually. Notably, the Korean Society of Medical Oncology and the Korean Association for Lung Cancer have participated in an integrated publication with CRT since March 2012 and March 2013. Cooperation with the related academic societies has aimed to contribute to the development of CRT. Therefore, the past 50 years could be roughly divided into three periods: the first period when research output increased with the development of academia (before the early 2000s); the second period when the importance of international indicators emerged but research stagnated before SCIE registration (from the early 2000s to the mid-2010s); and the third period of regrowth when research output increased since after SCIE registration and integrated publications with related oncologic societies (mid-2010s and onward). Notably, during the regrowth period since after the SCIE registration, significant growth occurred not only in the research quantity but also in its quality. This included an increase in multicenter, prospective, and randomized studies as well as more overseas submissions and fewer case reports. However, the quantitative growth of research during this period was primarily driven by an increase in clinical research; it is somewhat disappointing that the amount of preclinical research did not increase significantly. During the regrowth period, the proportion of research in internal medicine, including medical oncology, increased significantly. This is likely because of the rapid development of systemic treatments such as targeted agents and immunotherapy over the past 10 years. Additional efforts are needed in other fields, such as radiotherapy and surgery, where industry-academia cooperation is relatively lacking compared to technological advancements. Furthermore, although overseas submissions have been increased, vast majority has been contributed by China; hence, efforts are required to enhance the international influence of CRT.

Since its registration in SCIE, CRT has achieved remarkable growth. However, despite the steady growth of the journal’s impact factor, the percentile within the field remained at the 51%-66% after reaching its peak at the top 25.1% in 2015 (Fig. 10). Recently, CRT has achieved significant growth in clinical research, however, further growth by targeting the top quartile of international journals is necessary. To achieve this goal, CRT should consider publishing reviews or research methodologies by promising scholars and papers [6]. Clinical researches must continue to improve its quality following current trends. Additionally, utilizing domestic research groups to publish systematic literature analyses or clinical guidelines may be helpful. For example, the Oligometastasis Research Group under the Korean Cancer Society published three systematic literature analyses in CRT between 2023 and 2024 [7-9], which inspired oncologists and suggested new treatment strategies. Although the number of systematic reviews in CRT is small, it is encouraging that systematic literature analysis has increased in the last decade.

This study had several limitations. Some studies were difficult to clearly classify into one subject or design, and the three researchers who collected the data may have differed in their opinions. In the previous report [5] analyzed publications from 1970 to 2003, clinical studies were categorized in more detail as case-control studies, cohort studies, and phase 1, 2, and 3 studies. However, in this analysis, several studies could not be clearly classified using these categories except those related to new drug development. Considering that most clinical studies in fields other than internal medicine are retrospective observational, a simplified classification system was used to categorize the studies as randomized studies, nonrandomized control studies, case studies, or case reports. This simplified system was also used to reduce differences in opinions between the investigators. Since we classified studies in which the authors did not belong to a single institution as multicenter studies, studies in which the main data (e.g., patient records or experimental data) were provided by a single institution were also classified as multicenter studies, if authors from other institutions participated (e.g., writing the manuscript or data analyses). This classification may be somewhat different from the general concept of distinguishing between multicenter and single-center studies. This study included all publications (except withdrawn manuscripts) because it aimed to identify trends including all types of research, such as letters or reviews with academic value, systematic reviews, guidelines, or surveys. The analyses from 1970 to 2003 [5] and from 2004 to 2013 [10] included only original articles; therefore, the figures from this study may show slight differences.

After its founding, CRT underwent a developmental period in the 1990s and stagnated before SCIE registration. Over the last 10 years, with the help of SCIE registration, CRT has undergone rapid development, with significant qualitative and quantitative advancements. Although CRT’s impact factor has steadily increased, the percentile within the field requires further improvement. To make further progress, continuous enhancement of the quality of clinical research, encouragement of preclinical research, and the publication of methodological studies, review articles, and systematic reviews by active research groups are needed.

Article information Continued