Key Points

• The result of this research about the 100 most cited articles on breast cancer may help to understand important studies on breast cancer and shed light on future studies.

Introduction

Breast cancer is the most prevalent cancer globally, as well as a leading cause of cancer-related death among women (1).  Substantial support for breast cancer awareness and research funding has helped created advances in the diagnosis and treatment of breast cancer (2). Early detection, a novel personalized approach to treatment, and a better knowledge of the disease have all contributed to an improvement in breast cancer survival rates and a steady decline in the number of deaths related with the disease (3). Current guidance on preventing and treating breast cancer, as well as what might cause it, has come mainly from information discovered from research studies (4). The most significant component of the methodological qualities of studies is associated with an increase in citations and a high impact factor of the journal in which it was published (5). To the best of our knowledge, there is only one early study that has performed a bibliometric analysis of the attributes of the 100 most cited articles about studies concerning breast cancer (6). The aim of this study was to evaluate the current status of the 100 most frequently cited articles.

Materials and Methods

A Web of Science (WOS) (Clarivate Analytics, Philadelphia, PA, United States) search was used to collect the information for this investigation. The journals indexed in the Science Citation Index Expanded (SCI-E) were included. There were no restrictions on the journals. Over 9200 of the world’s most influential publications from 178 scientific areas are now indexed in the Science Citation Index Expanded™. More than 53 million records and 1.18 billion cited references date from 1900 to the present (7).

Inclusion Criteria

The term “breast cancer” was typed into the search box of WOS basic research with the selection of all the years and the search was performed on 11.02.2022. The search produced 621,351 published articles between 1978 and 2022. As filters, English language, SCI-E scope and research article type were selected, resulting in a reduction to 376,105 articles. These were then ranked in order of citation frequency, from highest to lowest. The study was conducted by generating a shortlist of the top 100 cited publications from this search list, which were classified by journal, study category, country and location where the research was published, authors, and publication date.

Exclusion Criteria

Articles in indexes other than SCI-E, published in languages other than English, and other types of articles, such as reviews, meeting abstracts, letters, book chapters, etc., were excluded. Also, cancer statistics articles were excluded, despite receiving more citations than the included research articles.

Written informed consent was not necessary because no patient data was included in the study. The study complied with the Declaration of Helsinki.

Statistical Analysis

No inferential statistical analysis was undertaken. All the data is given in percentages, numbers and charts.

Results

The articles included in the study are listed according to the total number of citations in the WOS database and in the all databases (WOS database, Arabic Citation Index, BIOSIS Citation Index, Chinese Science Citation Database, Data Citation Index, Russian Science Citation Index and SciELO Citation Index). According to our results, the most cited article was by Charles M. Perou and his colleagues, with 10,236 citations in the WOS database, and the least cited article was by Lisa A Carey and her colleagues, with 1,403 citations. Considering the number of publications, the most cited author was D.J. Slamon with 25,000 citations, followed by B. Fisher with 11,809 citations, T. Sorlie with 11,343 citations, Charles M. Perou with 10,236 citations, and N.K. Aaronson with 9247 citations (Table 1). It was evident that all articles received more than 1000 citations and all were published between 1985 and 2021. Twelve of the most cited articles were published in 2007, and there was one publication each for 1987, 1992, 1993, 1995, 2000, 2018, and 2021 among the most cited articles (Figure 1).

These most cited articles were published in 20, high-impact factor journals, with 24 articles published in the New England Journal of Medicine, 13 in Nature, 11 in the Journal of Clinical Oncology, and 11 in Science (Table 2). Seventy of the studies originated from the United States of America (USA), 13 publications from the United Kingdom (UK), six from Italy and three from Canada (Figure 2).

The articles were sourced from 51 different centers. The institution with the most publications was Harvard University with eight articles, followed by the University of Pittsburgh with six articles, the IRCCS European Institute of Oncology (IEO) with five articles, and the University of North Carolina with five articles, while 32 institutions had only one publication each (Table 3).

According to WOS publication categories, 37% of the articles were in the field of medicine, general and internal medicine, medicine, research & experimental, cell biology; pathology and surgery were the least published categories in this list. In addition, when the categories we created according to the content of the articles were examined, most articles were on genetics and drug research (47% and 24%, respectively) (Table 4).

Discussion and Conclusion

Citation analysis is used to find important papers on a certain subject. It aids in the analysis of scientific influence while also acknowledging substantial/pioneering contributions made by predecessors and noteworthy research advancement. There are numerous bibliometric article analyses conducted in various areas of medicine (8, 9, 10, 11).  To the best of our knowledge, there is only one previous article about the 100 most cited articles concerning breast cancer, and it was published in 2017 (6). Since research areas can change due to advances in science and technology, we found that the total number of citations in this study, which we aimed to evaluate the current status of the 100 most frequently cited articles, reached 280,906, an increase of approximately 1.6 times compared to 2017. This result suggests that interest in quality publications on breast cancer has increased. Also, 41 of the articles in the list were found to have changed. The vast majority of articles on the list were on chemotherapy and genetic studies.

The number of citations may be related to the time since publication. As the publication time increases, the number of citations also increases. In our study, we observed that 12 articles from 2007 and 9 articles from 2005 entered the list (Figure 1). However, many factors, such as the content of the article, its quality and the journal in which it was published, can affect the number of citations. Therefore, although it was published in 2021, the study by Xi Wang and his colleagues was the fourth most cited article (6).

As expected, the most cited articles were published in the medical journals with the highest impact factors. In the present study, most articles were published in the New England Journal of Medicine, followed by articles in Nature, the Journal of Clinical Oncology, and Science, respectively. The first three articles on the list were published in Nature, Science and the Journal of the National Cancer Institute, respectively. It is feasible to hypothesize that the audience of a general medical journal is particularly interested in the topic of breast cancer, or that authors of breast cancer research choose popular medical journals to reach more researchers and readers. One of the important points in the study was that 70% of the articles originated from the USA. Similar to our study, in the bibliographic studies in the literature, 70%–93% of the research articles were USA based (8, 9, 10, 11). The fact that these quality studies originate from the USA can be explained by the large patient population and the presence of many well-funded cancer centers.

The first most cited article was “Molecular portraits of human breast tumours” written by Perou et al. (12) in 2000. In this study, in which they made a molecular portrait of breast cancer, they created a molecular subtype classification of breast cancer (12). Today, this molecular classification is still in use and therefore the topic of this article remains relevant.

The second most cited article was “Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene” written by  Slamon et al. (13)  in 1987. In this study, they showed that the HER-2/neu oncogene may play a role in the biological behavior and pathogenesis of human breast cancer. Also, they found that amplification of the HER-2/neu gene is an important predictor of both overall survival and time to relapse in patients with breast cancer, and that the HER-2/neu oncogene plays a role in the biological behavior and pathogenesis of human breast cancer.

The third most cited article was “The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology” written by Aaronson et al. (14) in 1993. The EORTC QLQ-C30 questionnaire was developed as a reliable and valid measure of cancer patients’ quality of life in multicultural clinical research settings in this multicenter survey performed by the European Organization for Research and Treatment of Cancer.

The other most cited articles are in the fields of chemotherapy, gene expression, tumor genetics, pathology, and surgery. Research in these areas has made important contributions to the understanding of breast cancer. According to WOS categories, 91% of the articles were in the field of general internal medicine, multidisciplinary sciences was the second most common category, and cancer research came third. Surgery was one of the least-published fields. As the biological behavior and pathogenesis of breast cancer are better understood, studies on chemotherapy drugs have come to the fore. A possible reason for the increase in these types of studies is the increase in funding for drug research in the treatment of breast cancer. For this reason, research on surgery may have lagged behind.

Although citation analysis is a useful method that can provide insight into trends in the literature, it is not without flaws. Only the WOS database was used in this study. Thus, publications that may be indexed in other databases, such as Scopus and Google Scholar, were not included in the list of this study. Also, self-citations, lectures and textbooks were not evaluated. A search was made by typing only the term “breast cancer” in the WOS search box. Other terms that may be related to breast cancer, such as “breast, breast neoplasm, breast surgery, etc.,” were not searched. Another limitation was that the research area was examined according to the research categories determined by WOS. A more detailed investigation could not be made.

In conclusion, in this study, in which a bibliographic analysis of the 100 most cited articles in WOS on breast cancer was performed, it was observed that the number of citations increased by 1.6 times in the last 5 years. It was found that the most cited articles were published in high impact factor journals, especially the New England Journal of Medicine, most publications were from 2007, and the most cited articles were from the USA and Harvard University. Most studies focused on gene expression and chemotherapy. The result of this research may help to understand important studies on breast cancer and shed light on future studies.

Ethics Committee Approval: No ethical approval was obtained because this study did not involve a prospective evaluation, did not involve laboratory animals and only involved non-invasive procedures (e.g. faecal samples, voided urine etc).

Informed Consent: N/A

Peer-review: Externally peer-reviewed.

Financial Disclosure: The authors declared that this study received no financial support.