Physiologic functions of lymphatics and lymph node (LN) include tissue homeostasis, fluid balance, immune function, absorption of dietary fat, and lipid transport. However, they are of particular interest to oncologic surgeons because they are also involved in cancer progression. Metastatic initial events of the solid tumors are presumed to occur through the lymphatic system, though the role of metastatic LNs in cancer progression is not yet fully understood [12]. Whatever the role is, surgeons have concentrated clinical efforts to remove and analyze regional LNs after Halsted performed radical operations involving LNs in breast cancer patients in 1894 [3]. Doubtlessly, research on LNs and their relevance to cancer must have evolved ever since, reflecting various clinical and nonclinical developments that have influenced researchers. However, to the best of our knowledge, nothing has been said about how the research on cancer-related LN has evolved over the years.

Lately, with the advancement of the internet and computerized information, biomedical databases such as PubMed, Scopus, Web of Science, and Google Scholar have been extensively exploited. As Wormell [4] noted, online databases are not only about accessing documents and finding facts but also about tracing trends and developments in society and scientific disciplines. Indeed, recent works by information scientists have analyzed and organized preexisting medical knowledge using informetrics and linguistic analysis proving their usefulness [567].

In this article, we attempt to trace the trends of research conducted over the past several decades on cancer-related LN by exploiting the techniques used in informetrics. The results obtained will not only fill the void that has been formed and left untouched since the connection between LN and cancer was made by Halsted, but also provide potentially useful information for researchers and clinicians.

This study was exempted from the ethics approval and written informed consent from the participants from the Institutional Review Board of Jeonbuk National University Hospital (No. 2019-05-067).

As shown in Fig. 3, the United States produced the largest number of publications on cancer-related LN, followed by Japan, China, the United Kingdom, and so on. However, if we consider the incremental trends of articles over time, 2 countries stood out; China and South Korea. Their contributions increased significantly since 2007, compared to other countries. Especially, China showed a remarkable growth, publishing more articles than the United States since 2014. This is likely due to China's dramatic increase in investment in research and development (R&D). According to the latest available data on investment in R&D for Organisation for Economic Co-operation and Development (OECD) countries and other major economies published in the OECD's Main Science and Technology Indicators [10], gross domestic expenditure on R&D in China rose by 291% in 2015 compared to 2007. Likewise, South Korea's 180% increase in expenditure on R&D in the same period coincides with the rise in its contribution to the research on cancer-related LN. A rise in the expenditure on R&D appears to be a necessary condition for a rise in publications but not a sufficient condition. This means, in other words, that without a rise in the expenditure on R&D, there would be no rise in publications. This is indeed what happened to the United States. According to the National Cancer Institute report, they reduced funding for research on breast, lung, prostate, and colorectal cancer during the years of 2011–2016 [11]. This cut in funding directly corresponds to the line, which represents the United States in the graph of Fig. 3B, starting to flatten or decline in the early 2010s.

In addition to outlining the rise and fall of research articles in number with regard to variables such as time, place, and publisher, we investigated how research on cancer-related LN has evolved in their content by tracing the occurrences and distributions of 6 keywords; metastasis, dissection, sentinel LN, LN ratio, LN count, and micrometastasis. As is well known in the literature, it has been always at the center of attention in the literature to understand the process of LN metastasis and to identify the implications of LN dissection. Hence, there are the 2 keywords-metastasis and dissection. Sentinel LN is the first LN drained from a primary carcinoma [1213], and it is known to have 2 roles, “incubator” and “marker,” in cancer metastasis and progression [14]. Even though the 3 keywords of LN ratio, LN count, and micrometastasis are less pervasive terms than the other keywords in the literature, they appear in researches to complement the Union for International Cancer Control TNM stage [15] which is widely used for prognosis prediction.

The amount of articles on LN metastasis was found to be the greatest and steadily increasing over time. The increasing slope of the cancer-related LN articles in Fig. 2B shows a pattern similar to the slope of LN metastasis. Because LN metastasis is the basis and core of cancer-related research, related articles continue to emerge.

LN dissection is still considered to be the most effective treatment for most solid tumors [1416]. Despite the steady increment of the amount of research on LN dissection over time, its normalized frequency in Fig. 5C shows that the upward trend leveled off after 2000. This is presumably due to a disagreement among surgeons. While all oncologic surgeons agree that LN dissection is necessary for cancer surgery, they disagree as to the extent to which LN dissection is performed [17]. Sentinel LN attracted explosive interest from the late 1990s but the interest tapered off since the early 2000s. It was once considered as an innovative way to cope with extended LN dissection [1819]. But since then, the driving force behind the research has weakened because the accuracy and usefulness of sentinel LN in other solid tumors, except for breast cancer, was poor, and clinical application was limited [20].

LN ratio and LN count had hardly been discussed, but after the mid-2000s there was a slight increase in the amount of research on the subjects. By contrast, micrometastasis have still not attracted much attention in the literature. Apparently, the research field of sophisticated prognostic indicators such as LN ratio, LN count, and micrometastasis needs to gain new momentum to establish itself as one of the popular research fields.

For our analysis, we used informatics and linguistic filtering methods to articulate the trends. Admittedly, there are some limitations inherent to the methods we adopted, because it only allows us to trace, categorize, and count the words in the titles and abstracts of an article, rather than interpret their meanings in the context in which they are used. These limitations, however, do not undermine our research purpose in any significant way, since our aim here is to trace the general contour of the paths that a large number of articles have taken over a long period.

In conclusion, although research on cancer was abundant, only a small portion was dedicated to investigating its relevance to LN. Western countries had led the research on cancer-related LN, but Asian countries began to participate as major players, expanding their contributions. While LN metastasis, one of the major cancer-related LN topics, showed a steady increase, those involved in oncologic surgery such as LN dissection and sentinel LN did not.