Top 100 cited classical articles in sentinel lymph nodes biopsy for breast cancer

Background: The sentinel lymph node biopsy (SLNB) takes on a critical significance in breast cancer surgery since it is the gold standard for assessing axillary lymph node (ALN) metastasis and determining whether to perform axillary lymph node dissection (ALND). A bibliometric analysis is beneficial to visualize characteristics and hotspots in the field of sentinel lymph nodes (SLNs), and it is conducive to summarizing the important themes in the field to provide more insights into SLNs and facilitate the management of SLNs.

Materials and methods: Search terms relating to SLNs were aggregated and searched in the Web of Science core collection database to identify the top 100 most cited articles. Bibliometric tools were employed to identify and analyze publications for annual article volume, authors, countries, institutions, keywords, as well as hotspot topics.

Results: The period was from 1998 to 2018. The total number of citations ranged from 160 to 1925. LANCET ONCOLOGY and JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION were the top two journals in which the above articles were published. Giuliano, AE was the author with the highest number of articles in this field with 15. EUROPEAN INST ONCOL is the institution with the highest number of publications, with 35 articles. Hotspots include the following 4 topics, false-negative SLNs after neoadjuvant chemotherapy; prediction of metastatic SLNs; quality of life and postoperative complications; and lymphography of SLNs.

Conclusion: This study applies bibliometric tools to analyze the most influential literature, the top 100 cited articles in the field of SLNB, to provide researchers and physicians with research priorities and hotspots.

1 Introduction

Breast cancer has become the disease with the highest morbidity and mortality among women in most countries (1). The axillary lymph node (ALN) status is one of the most important indicators for evaluating the prognosis of breast cancer (2), and axillary lymph node dissection (ALND) has always been considered the gold standard for assessing the metastasis of ALNs, and it has been commonly employed in the surgical treatment of breast cancer. However, as a result of the obstruction of the axillary lymphatic system easily by axillary surgery, which can result in a series of complications (e.g., lymphedema of the affected limb, limited shoulder joint movement, and decreased muscle strength (3–5)), ALND has resulted in great inconvenience to the patients in postoperative life.

With the improvement of early diagnosis and comprehensive treatment of breast cancer, de-escalation has been more generally recommended as the surgical treatment of breast cancer. A considerable number of researches have confirmed that the sentinel lymph node (SLN) of breast cancer is the first-stop lymph node draining the primary tumor, as well as the first-stop lymph node draining the entire breast organ (6, 7). Since this concept has been progressively recognized, sentinel lymph node biopsy (SLNB) has been extensively employed in clinical trials. SLNB can accurately stage the ALN status of breast cancer (8–12) while effectively reducing the incidence of postoperative complications (13–17). It has replaced conventional axillary surgery and become the standard surgical treatment for early breast cancer (18, 19).

Bibliometric analysis is effective in investigating the development of a field and identifying vital research hotspots (20). It is imperative to use the bibliometric analysis that can provide various quantitative indicators of the number of publications, scientific achievements, and the effect of authors (21, 22) to identify the trends and hotspots of SLNB and then help scholars explore new directions for future researches in the academic realm.

2 Materials and methods

2.1 Data source

The publication on sentinel lymph nodes of breast cancer retrieved 7076 articles in the Web of Science core collection database (WoSCC) from 1998 to August 2022. The search strategy is presented as follows: “sentinel node*” or “sentinel lymph node*” or “sentinel lymphadenectomy” or “SLNs” AND “breast cancer” or “breast carcinoma” or “breast tumor*” or “breast neoplasm”. 3614 English articles were included. Lastly, the 100 most cited publications were collected. Two authors (Pengfei Lyu and Pingming Fan) assessed the retrieved data respectively to identify the literature relating to SLNB in breast cancer. If there are any opinions, another author (Ke Ma) will be consulted, and a consensus will be reached through discussion.

2.2 Statistical analysis

Data were input into the tools of bibliometrics. The analysis was conducted using RStudio (version 4.1.3), gCLUTO (version 1.0), and VOSviewer (version 1.6.14), which were adopted to build networks of bibliographic couplings based on keywords and co-occurrence analysis, among others for the visual analysis of the network.

3 Results

3.1 Main information

The period was from 1998 to 2018; the sources (journals) were 29; the average number of citations per document was 365.6; the average number of citations per document per year was 24.8. Article type: article 75; proceedings paper 18; editorial material 1; review 6.

The total number of citations ranged from 160 to 1925. The most cited articles have been written by Giuliano, AE, and so forth published in the JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION in 2011 on a comparative study of ALND and non-ALND in breast cancer with sentinel lymph node metastasis. The top 100 most cited articles in the field of SLNB for breast cancer are listed in Table 1. Table 2 lists the annual average citation (citation rate) of the top 10 articles relating to SLNB. Articles published by Giuliano, AE, and so forth occupied four of them, and the period was from 1994 to 2017. LANCET ONCOLOGY and JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION were the top two journals of the above articles published.

TABLE 1

Table 1 The top 100 most cited articles on SLNB.

TABLE 2

Table 2 Annual average citation (citation rate) of top ten articles related to SLNB.

3.2 Analysis of countries, authors, journals, and institutions

Figure 1 shows annual scientific production and annual average article citations. The scientific output of the top 100 most cited articles reached the top in 1999(n=10, Figure 1A). The average yearly number of article citations reached 80.8 in 2017(Figure 1B).

FIGURE 1

Figure 1 The map of annual scientific production and annual average article citations. (A) The annual scientific output of the top 100 most cited articles, (B) The average yearly number of article citations.

57 of the 100 articles originated from the US, accounting for 57%. ITALY is the second-largest country with 12 pieces, far less than the US. Figure 2A illustrates the cooperation network of countries. As depicted in the figure, there are more than half of the articles from the US, as well as the most relationships with the US. Thus, the distribution of highly cited articles centered on the US has taken shape.

FIGURE 2

Figure 2 (A) Country Cooperation Map. The color depth represents the number of documents sent. The red line represents cooperation between countries. The thicker the line, the more the connections will be. (B) The top 20 authors’ production over time. The light blue circle represents the total citation (TC) per year, and the dark blue represents the number of articles.

For the author, Giuliano AE has published 15 articles, followed by Hunt KK published 14 articles and Viale G published 10 articles. The top 20 authors’ production over time is shown in Figure 2B. High-yielding authors such as Giuliano AE and Hunt KK are also highly cited.

The most relevant sources (Top 20 journals) are presented in Supplementary Figure 1. To be specific, the JOURNAL OF CLINICAL ONCOLOGY and ANNALS OF SURGERY both published 16 articles, followed by the Journal of ANNALS OF SURGICAL ONCOLOGY published 13 articles.

The top 20 publishing institutions are displayed in Supplementary Figure 2. Since EUROPEAN INST ONCOL published the largest number of 35 articles, it was the institution that contributed the most to the research of the sentinel lymph nodes. MEM SLOAN KETTERING CANC CTR and UNIV TEXAS published 28 and 15 articles, respectively. The three-domain diagram of authors, institutions, and countries is depicted in Supplementary Figure 3. Most of the highly prolific authors and institutions are from the US and Italy.

3.3 Analysis of keywords, thematic terms, and hotspots clusters

Figure 3A presents the co-occurrence analysis profile of the keywords. The top ten frequency keywords are presented as follows: lymphadenectomy, biopsy, carcinoma, axillary dissection, surgery, breast cancer, validation trial, metastases or micro-metastases, multicenter. Hence, the above high-frequency keywords suggest that the research focus of the above 100 articles was on biopsies relating to sentinel lymph nodes, axillary lymph node dissection, multicenter clinical validation trials, and management of metastases or micro-metastases in axillary lymph nodes.

FIGURE 3

Figure 3 (A) The co-occurrence analysis profile of the keywords. The size of the node represents the frequency of occurrence. The same color represents the same theme. Connecting lines represent co-occurrence. (B) The distribution of high-frequency subject terms over time. Lighter colors represent higher frequency of occurrence, darker colors represent lower frequency of occurrence, and black colors represent a frequency of 0. (C) A thematic map of the SLNB. The horizontal coordinate represents the degree of relevance and the vertical coordinate represents the degree of development. (D) A heat map of the visualization of four clusters. The red color represents values in the original data, the dark color represents larger corresponding values and the white color represents corresponding values of 0.

To avoid the bias of keywords representing the topic of the article, I have researched the subject terms (title keywords and abstract keywords). Figure 3B presents the distribution of high-frequency subject terms over time. The main subject terms were distributed year by year. We found that the main subject words occurred with high frequency from 1998 to 2013.

A thematic map of the SLNs is shown in Figure 3C. Basic themes are located in the lower right quadrant, including quality of life and complications after surgery; false-negative sentinel lymph node dissection; the impact of neoadjuvant chemotherapy on lymphatic imaging; and prediction of positive sentinel lymph nodes. The above small clustered themes are well-centered and poorly developed, suggesting that the above issues are extensively studied in the above 100 highly cited articles.

After the extraction of the subject terms and cluster analysis from 3 to 10, the result indicated that four clusters worked best, having the greatest in-group similarity and the smallest out-group similarity. The parameters related to four clusters are shown in the Supplementary Table 1. A heat map of the visualization of clusters is shown in Figure 3D. Using the semantics of the articles corresponding to the keywords we identified four major hotspots in SLNB research.

Cluster 0: False-negative sentinel lymph nodes after neoadjuvant chemotherapy

Cluster 1: Prediction of metastatic sentinel lymph nodes

Cluster 2: Quality of life and postoperative complications in sentinel lymph node biopsy versus axillary lymph node dissection

Cluster 3: Lymphography of the sentinel lymph nodes

4 Discussion

With a series of large samples of prospective clinical research on SLNB over the past few years, this operation has more crucial means for patients to assess lymph nodes status, staging, treatment plan formulation, and prognosis judgment of breast cancer and represents the development level of breast surgery to a certain extent (23, 24). There are considerable articles on sentinel lymph nodes from 1998 to 2022. In the above thousands of documents, many researchers have made outstanding contributions to the treatment of breast cancer, solved many clinical problems, and benefited most patients with breast cancer. In this study, bibliometrics was adopted to summarize the 100 most cited articles relating to SLNB. Moreover, characteristics, current hotspots, and possible trends can be assessed through the study of authors, countries, institutions, magazines, keywords, and so forth. Although most articles still use total citations to sort articles, there is a certain deviation in the early cited articles because they are time-dependent (25–27). Some literature is published in the recent period, whereas the number of citations is not enough to reflect the importance, and the articles with high citation rates are always worth exploring. Accordingly, we also analyzed the citation rate of articles (the average citations per year).

There is frequent cooperation between the US and European countries. The US not only accounts for a large proportion of the top 100 most cited articles. Most of the authors and institutions with great achievement come from the US, indicating that the US has made significant contributions to the research relating to SLNB in breast cancer and significantly affects the whole world. In terms of the research on reasons, the US government has given great financial support to sentinel lymph node researchers. The top 10 funding agencies are listed in Supplementary Table 2. Analysis of the keywords in the 100 most cited articles resulted in four major clusters, as follows.

Cluster 0: False-negative sentinel lymph nodes after neoadjuvant chemotherapy

Neoadjuvant chemotherapy (NAC) has been increasingly applied to locally advanced or early breast cancer to achieve the goal of radical or breast-conserving surgery at the lower stage. For patients without clinical metastasis of ALNs after NAC, the detection rate of SLNs accounted for 96%, the accuracy rate reached 99%, and the false negative rate (FNR) was 6%, similar to the FNR of SLNB in patients with early breast cancer who were not eligible for NAC (28). In other words, SLNB is adequately safe and feasible after NAC in this part of patients. For patients with clinical metastasis of ALNs, NAC may cause lymphatic vascular obstruction or fibrosis that changes the lymphatic drainage pathway, thus increasing the FNR of SLNB and affecting the judgment of tumor staging (29). Accordingly, ALND continues to be the standard treatment of patients whose metastatic ALNs disappeared by palpation and imaging assessment after NAC in routine clinical practice. Following the clinical guidelines, the FNR of SLNB should be lower than 10% (30), and on the premise of meeting this requirement, false-negative events may not affect the prognosis of patients after surgery (31). A meta-analysis enrolling 1521 patients who underwent SLNB or ALND after NAC in 23 articles showed that the accuracy rate of SLNB in evaluating the status of ALNs status was 89%, and the FNR was 13% which was higher than the threshold of 10% (32). As revealed by the results of relevant clinical trials, the FNR can be reduced to a certain extent by placing marker clips in lymph nodes before NAC, using ultrasound and other auxiliary examinations to assist in assessment before the operation, using the dye and nuclide dual tracer technology to map SLNs and increasing the number of SLNs during operation, as well as using immunohistochemical detection and defining the concept of SLNs strictly (33–38). However, the number of SLNs detected cannot be accurately predicted in clinical practice, the application of nuclide is limited, and even the clips placed by some patients may not be identified during the operation and others. As a result, other technologies (e.g., the application of targeted axillary lymph node dissection combining SLNB with marked lymph node biopsy (39)) and novel tracers (e.g., superparamagnetic iron oxide (40) and carbon nanoparticle suspension (41)) should be developed to provide the possibility for the safe use of SLNB in patients with clinically positive ALNs turning into negativity after NAC.

Cluster 1: Prediction of metastatic sentinel lymph nodes

Due to a considerable number of factors for the FNR of SLNB (42), many scholars have also tried to establish models for predicting metastatic SLNs, to select patients who are necessary to perform ALND after SLNB. The bibliometric analysis indicates that the nomogram is the main form of model construction, and the analysis of the above articles indicates that the size of the primary tumor, the number of SLN macrometastases and positive SLN resections, and peripheral vascular invasion are critical factors for additional metastasis of ALNs (43–49). The role of SLNB at the time that the risk of invasive disease on final pathology in patients with an initial diagnosis of ductal carcinoma in situ (ductal carcinoma in situ, DCIS) was sufficiently high and has not been well defined. The result of the study in the bibliometric analysis indicated that 55 years of age or younger, diagnosed by needle core biopsy, mammography with a size of at least 4 cm and high-grade DCIS were more likely to develop into invasive cancer. The presence of comedonecrosis and larger tumor sizes were the independent predictors of patients receiving SLNB, whereas the accessibility of the tumor was the only independent predictor of positive SLNs (50). Therefore, SLNB should not be performed routinely in all patients initially diagnosed with DCIS.

Cluster 2: Quality of life and postoperative complications in sentinel lymph node biopsy versus axillary lymph node dissection

ALND is the most accurate method to assess the status of ALNs in breast cancer, whereas it is also the main cause of postoperative complications (e.g., edema of the upper limb, pain, sensory and motor dysfunction). Since the screening methods for breast cancer are progressively enriched, the detection rate of early breast cancer increases year by year, and the proportion of new cases of breast cancer without the metastasis of ALNs also rises. If ALND is performed on all patients, most patients are excessive diagnosis and treatment, thus significantly affecting their quality of life and causing greater psychological stress.

Among the top 100 most cited articles, numerous articles have compared the complications and the quality of life of SLNB and ALND. The most cited and representative clinical trial called the ALMANAC trial showed that the postoperative situation of patients performing SLNB was superior to that of patients performing ALND in lymphedema, sensory disturbance, wound drainage, length of hospital stays, upper limb functional index, postoperative motor function recovery and mental illness (51, 52). A recent meta-analysis including 67 articles showed that SLNB was significantly lower than ALND in the prevalence of lymphedema and pain, and was also better than ALND in the range and strength of the affected limbs (53). In addition, a small-scale prospective clinical trial in the bibliometric statistics only reported the complications of SLNB which could not also be ignored. The article highlighted that older age and more SLNs resection are capable of increasing the incidence rate of axillary seroma, whereas this cannot affect the choice of axillary surgery for elderly patients with breast cancer and increase the number of SLNs dissection to reduce the false negative rate for surgeons (54).

Complications (e.g., lymphedema) can be currently treated by further surgery and should be consistent with the principle of prevention first and treatment as a supplement due to the difficulty of implementation and relatively high cost and long duration (55, 56). In brief, clinicians have sufficient evidence to consider that SLNB should be employed as the optimal operation for breast cancer patients with clinically negative ALNs.

Cluster 3: Lymphography of the sentinel lymph nodes

With the continuous development of lymphography technology of SLNB in breast cancer, people can easily understand the drainage pattern of SLNs and increase the detection rate of SLNB through this way. In the bibliometric analysis, more articles have focused on lymphography combining different imaging systems with an injection of indocyanine green and confirmed this method was feasible and safe for intraoperative SLNB and could be observed in real time without long-term training (57–61). Furthermore, novel tracers and relevant imaging systems (e.g., axillary ultrasound, and computed tomography lymphography) to locate and visualize positive lymph nodes in different ways can be adopted to guide the implementation of SLNB in clinical practice (62–64).

The lymphography of the SLNs is still in the experimental stage and needed to assess and confirm by more and further clinical articles. Although this technology enhances the ability of lymph node drainage, it may complicate subsequent surgery and radiation therapy. According to the results of the research by Jung et al., the use of indocyanine green fluorescence plus radioisotope dual imaging can also improve the detection rate of SLNs after NAC (65). Consequently, the lymphography of the SLNs may not be necessary and the FNR can still be effectively reduced by using the double-tracer method of different tracers.

5 Limitations

Firstly, only a single database was included in the bibliometric analysis which resulted in incomplete search results. Secondly, the retrieved articles only included English language literature. Thirdly, articles from the last few years have low citation rates due to their recent publication, but this does not mean that they are not important. Despite the above limitations, the analysis of this study provides insights into current controversies and future research directions for SLNB.

6 Conclusion

In this study, the top 100 most cited articles on SLNB for breast cancer were analyzed through bibliometrics in combination with network visualization analysis. Notably, the US was the leading country of most cited articles, and the research hotspots focused on the quality of life and complications after surgery, the impact of neoadjuvant chemotherapy on the false-negative rate of SLNB, lymphography, and prediction of metastatic SLNs. Future research directions may include decreasing the false-negative rate and increasing the accuracy of SLNB to expand its indications through the continuous development of advanced lymphatic imaging and mapping techniques and the establishment of reasonably predictive models of lymph node metastasis.

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding authors.

Author contributions

P-FL and PZ designed the study. KM and X-CC conducted a literature search. P-FL, PZ, KM, and X-CC analyzed data and wrote this thesis. All authors contributed to the article and approved the submitted version.

Funding

The study was supported by the Hainan Provincial Key Research and Development Program Project Fund (No. ZDYF2021SHFZ248).

Acknowledgements

Thanks to these authors: Xinrui Liang, Yu Wang and Guanghua Fu for their contributions to this article.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fonc.2023.1170464/full#supplementary-material

Supplementary Figure 1 | Most relevant sources (top 20 journals).

Supplementary Figure 2 | The top 20 publishing institutions.

Supplementary Figure 3 | The three-domain diagram of authors, institutions, and countries. The size of the squares represents the number of articles published, and the linking lines to each other represent attribution.

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