The incidence of human cancer is increasing worldwide. It is estimated that the global burden of cancer will increase by more than 60% by 2040 [1]. Cancer has been an important public health problem in low- and middle-income countries, as well as in upper-middle-income countries. Cancer research has become one of the leading research fields of bioscience around the world, and the number of publications on cancer increases at a rate of more than 2% per year [2].

A high-quality cancer database can provide researchers with convenient data analysis and build a sharing platform among researchers, which could pave the way for revealing the mechanism of tumorigenesis and its progression [3]. To share clinical data with different regions, some other countries plunged into building multicenter databases far ahead of China [4]. In 1973, the US National Cancer Institute combined the tumor registration stations in several regions to form the Surveillance, Epidemiology, and End Results (SEER) database. The SEER program is a globally accessible authoritative cancer database representing approximately 34.6% of the US population, which includes non-Hispanic White, non-Hispanic Black, Hispanic, and Asian populations [5]. The SEER program collects data on patient demographics, tumor location, tumor stage, first course of therapy, and vital status. The SEER database is a valuable, population-based resource that can be used to study the diagnosis and treatment across demographic characteristics and geographic areas, and it has become a unique research resource for oncology practice. It provides morbidity and mortality data on various histopathological subtypes, and data on molecular characteristics are also expanding. The database is being further developed to capture other biomarker data and the results of specific populations, and to expand the biobank to support cutting-edge cancer research that can improve oncology practices. Therefore, the SEER program plays an important role in clinical cancer research, public health management, and policy making [5].

In recent years, China has made significant progress in clinical cancer research, and many studies have gained international recognition [6-10]. Although major hospitals have established databases in China, they have not shared their research findings with one another. Since the SEER database is a globally accessible authoritative cancer database, more and more scholars, particularly those from China, have used it to conduct clinical cancer research in recent years. There are a lot of differences between the United States and China, including their population’s genetic makeup, health system, health services, health insurance, health policies, socioeconomic status, and culture. Therefore, the research findings in the SEER cancer registries may not be generalizable to the people of China. However, several recent studies found that the characteristics of the data from the SEER program were consistent with those from Chinese institutions [11-14]. There is currently no comprehensive bibliometric study that has characterized the clinical cancer research in China based on the SEER database. Carrying out a comprehensive bibliometric analysis is helpful to analyze the contribution of Chinese scholars to clinical cancer research and provide a specific clinical reference for the future of big data analytics.

This study aimed to evaluate the characteristics of clinical cancer research using SEER data from mainland China using a bibliometric approach.

Using the search terms “Surveillance, Epidemiology, and End Results or SEER, and China,” we identified related publications from the PubMed database before August 31, 2020. PubMed is a free, publicly available database established by the US National Library of Medicine [15]. As one of the largest databases in the life science and biomedical fields worldwide, it comprises more than 30 million biomedical abstracts from journals and online books.

Publications with first authors or corresponding authors affiliated with mainland Chinese institutions were included in the study, while those that utilized the SEER-Medicare database (SEER-Medicare data are not released outside of the United States) and special types of publications, including comments, letters, and reviews, were excluded. Papers from Taiwan Province, Hong Kong, and Macao Special Administrative Regions were also excluded from this analysis. This study was approved by the ethics committee of the First Affiliated Hospital of Xiamen University (Xiamen, Fujian, China).

The indices analyzed in this study included the number and trend of publications, research topics, type of affiliation (university, hospital, or other research center), geographical distribution, journal, Journal Citation Reports (JCR) ranking, and status of international cooperation.

Descriptive statistical analyses were used in this study. Characteristics were evaluated and analyzed using Microsoft Excel, and linear regression was performed using SPSS statistical software (version 22.0; IBM Corp). P values <.05 were considered statistically significant.

The flowchart of publication selection for this study is shown in Figure 1. We retrieved a total of 1667 publications, of which 1566 publications were included in this study. Figure 2 shows the trend in publications on clinical cancer research using the SEER database in mainland China (R²=0.430, P<.001). Chinese authors first used the SEER database in 1999. The single paper in the SEER database that was published in 1999 was authored by Guo et al [16], who were affiliated with the People’s Hospital of Beijing Medical University and had collaborated with Huvos and colleagues from Memorial Sloan-Kettering Cancer Center in the United States. Interestingly, there were no papers from Chinese institutions that utilized the SEER database during the 11 years from 2000 to the end of 2011. However, the number of papers published per year increased rapidly from 2012 to 2019: 2012 (n=6), 2013 (n=12), 2014 (n=19), 2015 (n=43), 2016 (n=96), 2017 (n=181), 2018 (n=288), and 2019 (n=459). Despite the COVID-19 pandemic in 2020, there were 461 publications as of August 31, 2020.

Table 1 presents the main research topics of the 1566 papers included in the study. Breast cancer was the most frequently researched topic (213/1566, 13.6%), followed by colorectal cancer (185/1566, 11.8%), lung cancer (179/1566, 11.4%), gastrointestinal cancer (excluding colorectal cancer; 149/1566, 9.5%), and genital system cancer (93/1566, 5.9%). These top 5 research topics were the focus of 52.3% (819/1566) of the included papers.

Figure 3 shows the publication trends on the top 5 cancer sites in mainland China over time. It shows an increasing interest in research exploring breast cancer, lung cancer, gastrointestinal cancer (excluding colorectal cancer), colorectal cancer, and genital system cancer (in both genders). Chinese researchers were also studying rare cancers. A total of 164 papers discussed rare cancers, such as pulmonary lymphoepithelioma-like carcinoma, spindle cell carcinoma, thymoma, and adenoid cystic carcinoma of the breast, and this number was expanding rapidly in recent years.

Figure 4A shows the distribution of the publications using the SEER database whose first authors were affiliated with Chinese institutions. These first authors who used the SEER database to publish papers came from 25 provinces and municipalities of China. Among all of these regions, first authors were most often affiliated with institutions in Shanghai (369/1566, 23.6%), followed by Guangdong (199/1566, 12.7%), Zhejiang (174/1566, 11.1%), Hubei (102/1566, 6.5%), and Jiangsu (102/1566, 6.5%).

Figure 4B shows the distribution of publications using the SEER database whose corresponding authors were affiliated with Chinese institutions. These corresponding authors who used the SEER database to publish papers came from 27 provinces or municipalities of China. A similar distribution was observed in the papers whose corresponding authors were affiliated with Chinese institutions, mostly concentrated in Shanghai, Guangdong, Zhejiang, Jiangsu, and Hubei.

The top 10 affiliated organizations of the most contributing first authors and corresponding authors extracted from the 1566 publications are presented in Tables 2 and 3. More than 75% (1178/1566) of papers were published from the eastern coastal region of China, Overall, the organization that was affiliated with the top contributing first authors was Fudan University Shanghai Cancer Center (163/1566, 10.4%), followed by Sun Yat-sen University Cancer Center (73/1566, 4.7%), the First Affiliated Hospital of Xi’an Jiaotong University (48/1566, 3.1%), West China Hospital of Sichuan University (42/1566, 2.7%), the Second Affiliated Hospital of Zhejiang University School of Medicine (41/1566, 2.6%), and the First Affiliated Hospital of Xiamen University (41/1566, 2.6%). All affiliations of first authors extracted from the 1566 publications (excluding three papers whose first authors were affiliated with the United States) were classified into three sectors (university, hospital, and government agency). The most contributing institution sector was hospital (1501/1563, 96.0%), followed by university (60/1563, 3.8%), and government agency (2/1563, 0.1%). Of the 1501 papers from hospitals, 1459 (97.2%) publications were produced from the best tertiary hospitals, and 1475 (98.3%) were from hospitals affiliated with universities.

The organization that was affiliated with the top contributing corresponding authors was Fudan University Shanghai Cancer Center (165/1566, 10.5%), followed by Sun Yat-sen University Cancer Center (77/1566, 4.9%), Zhongshan Hospital of Fudan University (43/1566, 2.7%), the First Affiliated Hospital of Xi’an Jiaotong University (43/1566, 2.7%), and the Second Affiliated Hospital of Zhejiang University School of Medicine (42/1566, 2.7%). All affiliations of corresponding authors extracted from the 1566 papers (excluding 35 publications’ organization affiliations of corresponding authors affiliated with the United States, Germany, Australia, and Japan) were also classified into three sectors (university, hospital, and government agency). Similarly, the most contributing institution sector was hospital (1474/1531, 96.3%), followed by university (54/1531, 3.5%), and government agency (3/1531, 0.2%). In the 1474 papers whose corresponding authors came from hospitals, 1440 (97.7%) publications were from best tertiary hospitals, and 1458 (98.9%) were from hospitals affiliated with universities.

Overall, 267 journals were analyzed in the present study, of which the most contributing journal was Oncotarget (136/267, 50.9%), followed by Cancer Medicine (98/267, 36.7%), Journal of Cancer (76/267, 28.5%), Medicine (Baltimore) (72/267, 27.0%), and Cancer Management and Research (69/267, 25.8%). The JCR ranking was retrieved from Web of Science, a global citation database. The top 30 most common journals extracted from the 1566 publications are shown in Figure 5. The distribution of the JCR ranking of the 1566 publications is depicted in Figure 6. A total of 37.4% (585/1566) of the publications were published in the second quartile, followed by the third quartile (489/1566, 31.2%), first quartile (312/1566, 19.9%), unknown JCR ranking (100/1566, 6.4%), and fourth quartile (80/1566, 5.1%).

A total of 180 publications were jointly produced by organizations from China and 23 other countries including the United States (114/180, 63.3%), Russia (17/180, 9.4%), Italy (12/180, 6.7%), Australia (10/180, 5.6%), and Japan (10/180, 5.6%). Chinese institutions first cooperated with institutions from other countries using the SEER database in 1999. Similarly, no papers were jointly produced by institutions from China and other countries utilizing the SEER database during the 11 years from 2000 to the end of 2011. However, the number of papers produced through international cooperation increased substantially from 2016 (9/1566, 0.6%) to 2019 (65/1566, 4.2%). As of August 31, 2020, a total of 45 papers had been published in the year 2020 with international cooperation (Figure 7).

In conclusion, our study suggests that clinical cancer research regarding the SEER database has rapidly increased in China in the past decade. High-quality and national comprehensive cancer registries from China are needed to provide a reference for the future of big data analytics.