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Egyptian Journal of Radiology and Nuclear Medicine
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Mapping the landscape of Y90 radioembolisation research: a citation analysis of the top 100 papers

Egyptian Journal of Radiology and Nuclear Medicine volume 55, Article number: 169 (2024) Cite this article

Abstract

Background

This study aims to identify trends, research gaps, leading journals, institutions, countries, and authors by examining the top 100 cited Yttrium-90 Radioembolization (Y90) research articles. The insights gained will assist funding and collaboration efforts in Y90 research. The team analyzed 981 articles from 36 peer-reviewed journals, gathering data on authors, publication year, journal, citations, affiliations, keywords, and references. Author affiliations were scrutinized to pinpoint institutions and countries. p values < 0.05 were deemed statistically significant.

Main body of abstract

The most cited paper (703 citations) was authored by Salem et al. (2010), and the journal with the most publications (16) was Journal of Vascular and Interventional Radiology. There was no significant correlation between journal impact factor and citation metrics. A decreasing trend in the number of top 100 articles was observed since the peak period (2008–2013). Most papers were published in high-impact factor (IF > 3, n = 31/35) and SCImago Q1 journals (86/100), with Northwestern University, Clínica Universidad de Navarra, and Ludwig Maximilian University of Munich being the leading institutions. The most prolific authors were Salem, R., Lewandowski, R.J., and Mulcahy, M.F., with Salem, R. as the most influential. A statistically significant positive correlation between collaborative links and published articles was also discovered.

Short conclusion

The top 100 cited articles were primarily published in high-impact journals, and Northwestern University and the USA showed greater productivity and collaboration. These findings have crucial implications for researchers, policymakers, and institutions, aiding in the improvement of Y90 application and understanding in clinical practice.

Background

Yttrium-90 radioembolization (Y90) is a minimally invasive and targeted therapy that uses microspheres loaded with the beta-emitting radionuclide Yttrium-90 to selectively eradicate cancerous cells in the liver [1]. In recent years, Y90 radioembolization is a viable alternative to traditional therapies for primary liver tumors, including hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (ICC) [2], and liver metastases from breast, neuroendocrine, and colorectal cancers [3]. This treatment modality is relatively well-tolerated with low morbidity and mortality rates, making it a suitable option for patients who are not eligible for surgery or systemic chemotherapy due to underlying medical conditions or advanced stages of their illness [4].

Understanding the scientific landscape of Y90 radioembolization is crucial due to the increasing prevalence of liver malignancies worldwide [5] and the growing demand for treatment. This study examines the top 100 most cited articles on Y90 radioembolization to offer valuable insights into the evolution, advancement, and influence of research in this field using bibliometric analysis.

Bibliometrics utilizes statistical and mathematical methods to analyze scientific publications, allowing for the identification of patterns, mapping of scientific research evolution, and assessment of research impact in a particular field [6]. In Y90 radioembolization, comprehending breakthroughs, emerging patterns, and potential future directions is vital for researchers, healthcare providers, and policymakers. Although bibliometric studies have previously been conducted in interventional radiology and oncology [7], none have focused exclusively on Y90 radioembolization.

By examining the top 100 most cited publications on Y90 radioembolization, the study aims to identify the most significant authors, institutions, countries, and journals contributing to the field. It also explores research themes and trends over time, providing insights into the development of this treatment modality and its impact on patient care. Understanding key drivers and contributors will stimulate further research and development, leading to improved patient outcomes and a higher quality of life for individuals affected by liver cancer.

Materials and methods

This retrospective bibliometric analysis did not require ethical approval as it did not involve human or animal subjects. The study aimed to examine the top 100 most cited peer-reviewed articles on Yttrium-90 Radioembolization (Y90) up until March 31st 2023, using the Web of Science database [8, 9]. Two authors conducted separate searches to reduce bias, and any disagreements were resolved by consulting a third author.

We employed various search terms using the "Topic" field in Web of Science [8], searching for terms in the title, abstract, author keywords, and Keywords Plus. The search terms were “Yttrium 90 radioembolization” OR “Yttrium-90 radioembolization” OR “Y90 radioembolization". The search was limited to "articles" and produced 981 articles with no language or keyword restrictions. The top 100 most cited articles were selected for analysis without any exclusions, using citation counts according to the Web of Science [8] CORE number.

To account for temporal bias and citation lag, we also analyzed the top 10 articles from the last five years (2019–2023) that were not already in the top 100. We used the same search criteria as before and manually excluded articles already in the top 100 most cited articles.

Bibliometric data collection involved extracting various information types, such as authors, publication year, journal, citations, affiliations, author keywords, and references. Authors' affiliations were used to obtain information on institutions and countries, analyzed by VoxViewer [10, 11] and manually refined in Microsoft Excel [12]. Additionally, journal impact factors were obtained from the 2021 Clarivate "Journal Citation Reports" database [13] and the 2021 SCImago Journal Rank [14].

Data refinement and statistical analysis were conducted using a variety of software tools. Microsoft Excel [12] and Tableau [15] were used for data refinement, while Tableau [15], VOS Viewer [10, 11], and Web of Science [8] analysis tools were used for result visualization. R [16], specifically the Bibliometrix [17] package, was utilized for statistical analysis with the aid of Biblioshiny [18]. The Web of Science [8] dataset was uploaded to Biblioshiny [18] via R [16] for analysis.

Results

We analyzed 981 documents related to Yttrium-90 (Y90) radioembolization published from 1993 to 2023. Table 1 displays the top 20 studies along with information such as year of publication, average citations per year, journal title, JCR impact factor [13], and SCImago Journal quartile [14]. The full list of the top 100 can be found in Supplemental Table 1.

Table 1 Top 20 most cited papers on Y90 radioembolization (ranked by descending citation count)
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The most cited paper had 703 citations and reported long-term outcomes following Y90 radioembolization for patients with Hepatocellular carcinoma (HCC) [19]. The second and third most cited articles were [4] with 497 citations and [20] with 463 citations. The top 100 articles had a median of 108.5 citations, ranging from 69 to 703. The paper with the highest average citations per year (65.29) was published in "Lancet Oncology” [21]. The median average citations per year was 10.035, ranging from 4.18 to 65.29.

Out of the 36 journals examined, 9 had published four or more articles, accounting for 53 out of the top 100 most cited papers. Figure 1 illustrates the different journals along with citation metrics. The most prolific journal was "Journal of Vascular and Interventional Radiology" (JVIR), with 16 publications, a SCImago Quartile (Q) of Q1, and a JCR Impact Factor (IF) of 3.7. "Hepatology" had the highest number of citations, with 2201 in total, followed by JVIR with 1640. "Gastroenterology" had the highest average citations per paper, with an average of 496 citations for three papers published. Table 2 presents the detailed results. Most of the papers (86/100) were published in Q1 journals, with a minority being published in Q2 (12/100) and only one in Q3.

Fig. 1
figure 1

Journals ranked by number of documents. a On the left: journal’s and number of documents, b On the right: journals and total number of citations

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Table 2 Journals ranked by JCR impact factor
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The H-index [22] of each journal was equal to the number of articles published, since the lowest total citations (69) surpassed the highest number of articles (16) published by a single journal.

Three of the top 100 most cited articles were published in 2021 [23,24,25]. Figure 2 shows the distribution of articles published per year, with the most productive years being from 2008 to 2013, during which over eight articles per year achieved top 100 citation status. In the last five years (2019–2023), eight articles made it to the top 100, but none from 2022 or 2023 have achieved this status. Temporal bias and citation lag likely affect these results.

Fig. 2
figure 2

Number of articles publisher per year

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To account for temporal bias and citation lag, we analyzed the top 10 articles from the last five years (2019–2023) not already in the top 100. The results can be found in Supplemental Table 2.

All of these articles had an average citation rate per year of 5.8 or more [26, 27]. The "European Journal of Nuclear and Molecular Imaging" published three of the top 10 articles [26, 28, 29], highlighting its recent productive contribution to the field. While this suggests that these articles may enter the top 100 list, it's important to remember that citation rates can fluctuate over time [4].

For the top 100 most cited articles, the journal with the highest impact factor was "Lancet Oncology," with an IF of 54.433 and an average of 326 citations per paper[13] (see Table 2).

We found no significant correlation between impact factor and average citations per article (r2 = 0.14, p = 0.02), total citations (r2 = 0.05, p = 0.18), and number of articles published (r2 = 0.0005, p = 0.89), using a p-value of < 0.05 as the threshold for statistical significance (Fig. 3) [30,31,32].

Fig. 3
figure 3

Scatter plots. a On the top, number of documents versus JCR impact factor, b Middle, number of citations versus JCR impact factor, c On the bottom, average number of citations per paper published versus JCR impact factor

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We categorized journals into five groups: Radiology, Gastroenterology & Hepatology, Oncology, Surgery, and Other. Radiology journals published the most papers (40) across 12 journals, resulting in 4398 citations. Gastroenterology & Hepatology journals had the highest total citations at 5118, with 25 articles across eight journals. Oncology journals were the third most significant in terms of total articles and citations, with 20 articles across seven journals and 4216 citations. When considering average citations per article, Gastroenterology & Hepatology journals ranked highest with an average of 639.79, followed by Oncology (602.28), Radiology (366.5), and Surgery (306).

We used box and whisker plots (Fig. 4) to visualize the distribution of published articles and citations received by journal category.

Fig. 4
figure 4

Box and Whisker plots. a Top: subject of journal versus number of documents published. b Bottom: subject of journal versus total number of citations

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Radiology had the highest average number of articles per journal, with an Interquartile Range (IQR) ranging from 1 to 3.5 articles. JVIR was an outlier, having published 16 articles. In Gastroenterology & Hepatology, IQR ranged from 1 to 3 articles per journal with "Hepatology" as an outlier having published 8 articles. Oncology had an IQR spanning 1.5–4.5 articles with no outliers.

Oncology journals had the highest average citations per paper at 201. Gastroenterology and Hepatology journals averaged 157 citations per paper, with an IQR of 88 to 569. Two outliers in this category were "Gastroenterology" (1488 citations) and "Hepatology" (2201 citations). Surgery journals had an average of 155 citations per paper. Radiology journals had the lowest average citations per article (124) and an IQR of 168.5 to 325, with two significant outliers: "Cardiovascular and Interventional Radiology" (724 citations) and "Radiology" (1640 citations).

We found that 130 institutions contributed to the authorship of the top 100 most cited papers on Y90 radioembolization. Among these, 36 institutions contributed to three or more papers (Supplemental Fig. 1). Northwestern University had the highest number of documents (39) and total citations (7188), followed by Clínica Universidad de Navarra (CUN) with 13 documents and 2392 citations. The University of Illinois had the highest average citations per paper (251.5) for their four articles. Northwestern University had a relatively high average citations per paper of 184.3 for their 39 articles.

In this study, we used Links and Link Strength to assess collaboration. Links represent connections based on co-occurrence, while Link Strength indicates the connection's weight determined by co-occurrence frequency. These metrics help identify important patterns and connections within the data.

Northwestern University had the highest number of links (n = 64) with a link strength of 103. Clínica Universidad de Navarra (CUN) had the second-highest number of links (n = 61) with a link strength of 92. Figure 5 provides a visual representation of the collaboration network.

Fig. 5
figure 5

Collaboration network of institutions

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Our study categorized institutions into distinct clusters to investigate patterns of collaboration in Y90 research. Geographical location played a significant role in collaboration. East Asian and Oceanian universities dominated Cluster 1, while Cluster 2 was mainly composed of German universities. French universities were grouped in Cluster 3, while British universities formed Cluster 4. Italian universities were primarily included in Cluster 6. Clusters 5, 8, and 11 were predominantly composed of American institutions, while Cluster 7 exhibited a mix of European universities from various countries, such as Spain, Germany, Italy, and The Netherlands. Cluster 9 and 10 included a combination of European and American institutions, with "University of Hong Kong" also included in the mix. (See Table 3 for details).

Table 3 Institutions divided into collaboration clusters with relative links and link strength
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Sixteen countries authored at least two documents among the top 100 most cited on Y90 (Table 4). The United States was the most prolific contributor with 55 articles, followed by Germany (22), Australia (15), Spain (15), France (13), and Italy (12). These countries also had the highest total citation counts, with the United States having the highest at 9356, followed by Germany (3290) and Spain (2709) (Fig. 6).

Table 4 Countries ranked by number of Citations (included those with > / + 2 articles)
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Fig. 6
figure 6

World map with colour gradient indicating number of articles published

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Taiwan had the highest average citations per paper at 254, based on two papers. The United States had an average of 170 citations per paper, Germany 150, and Spain 181. The United States ranked fifth in terms of total links (20) despite contributing the most articles (55). Australia was the most collaborative country (26 links), followed by South Korea, Germany, France, Spain, Singapore, and Belgium. Germany had the highest link strength (63), followed by the United States, Spain, and France. Egypt and Grenada had one and two collaborative links, respectively (Table 4).

Salem, R. emerged as the most prolific author with 40 articles, 6838 citations, and an average of 170 citations per paper. Lewandowski, R.J. and Mulachy, M.F. were also notable contributors. Abecassis, M. had the highest average citations per paper (306) among ten documents. Figure 7 shows data for the 26 authors who published six or more articles, including the number of articles, citations, and average citations per paper.

Fig. 7
figure 7

Bar chart ranked by number of articles published by each author (including authors with >/=6 articles). a Authors versus number of published, b authors versus total number of citations, c Authors versus average citations per paper

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Fractional authorship was used to assess the authors' relative importance based on their contributions. Salem, R. had the highest fractionalized authorship score of 3.1/100, with Mulcahy, M.F. and Lewandowski, R.J. also exhibiting significant contributions.

Seven of the top 10 most productive authors, including the top four, were affiliated with Northwestern University. The remaining three were associated with USC, University of Zurich, and CUN.

We analyzed the citation data of the top 100 publications to determine the frequency with which authors were referenced by other publications in the top 100. Salem, R. was the most commonly referenced author with 252 citations. Lewandowski, R.J. and Mulcahy, M.F. followed with 186 and 163 citations, respectively.

The analysis of author productivity over time in the field of Y90 radioembolization reveals a decline in high-citation research output since 2013 (Fig. 2). This is likely influenced by citation lag but may also signify waning interest, challenges in innovation, or shifting research priorities. Salem, R. has maintained a consistent pattern of publication, with recent articles [23, 25] entering the top 100 most cited publications in the field (Fig. 8).

Fig. 8
figure 8

Author production over time (top 15)

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The most productive year was 2008, with 15 articles being published on Y90 radioembolization that are in the top 100 most cited. Many authors published over five articles that year, primarily due to collaboration on seminal articles that have become heavily cited over time [33,34,35,36,37].

Five authors had 25 links: Salem, R., Lewandowski, R.J., Mulcahy, M.F., Sato, K., and Gates, V.L., all affiliated with Northwestern University. Salem, R. had the highest link strength (240), followed by Mulcahy, M.F. (206) and Lewandowski, R.J. (201).

Furthermore, our analysis found a positive correlation between the number of links and the number of articles published by individual authors (r2 = 0.4, p = 0.0008), suggesting that collaboration is likely to be associated with increased publication output. This finding is intuitive, as collaboration can increase overall output by expanding capacity to do work.

Discussion

Our bibliometric analysis of publication records and citation metrics provides valuable insights into the field of Yttrium-90 radioembolization. By identifying research hubs and leading voices, our analysis can aid in directing funding and collaboration efforts.

The most cited study [19] significantly contributed to understanding Yttrium-90 radioembolization's long term efficacy in treating hepatocellular carcinoma (HCC). Its high citation rate indicates that it serves as a valuable reference for researchers and practitioners.

Nine journals accounting for 53 of the top 100 most cited articles, with JVIR, "Hepatology," and "Gastroenterology" making substantial contributions. Radiology journals had the highest number of published papers, while Gastroenterology & Hepatology journals had the highest total citations. This information can help researchers and institutions prioritize their reading and submission efforts to the most influential information sources in Yttrium-90 microsphere research.

As we demonstrated journal impact factors and no direct correlation with citation metrics and each has different relevance based on the circumstance [38, 39]. Thus a journal's impact factor alone is not a reliable indicator of scientific impact or exposure of articles, necessitating additional metrics and tools for a comprehensive evaluation of research quality and impact [38].

As shown by the high average yearly citation rates of recently published articles (2019–2023), Y90 research quality strong, requiring more time to overcome citation lag and be more widely recognised. These insights into temporal bias and trends enable stakeholders to allocate resources more effectively and support the continued advancement of this vital cancer treatment area.

Northwestern University, Clínica Universidad de Navarra, and Ludwig Maximilian University of Munich are highly productive in Y90 radioembolization research, indicating strong research environments, robust funding, and access to cutting-edge resources. Identifying such institutions helps researchers, funders, and policymakers understand key players and their contributions. For Y90 radioembolization researchers, these findings can guide institution selection for employment, collaboration, or training opportunities [40].

Geographical location plays a significant role in determining collaboration patterns among institutions, with the majority of collaborative clusters in Y90 radioembolization research being regionally focused [41, 42]. In the future, researchers in one cluster could collaborate with those in another cluster to share resources, expertise, and data, leading to new research projects and knowledge advancement [43].

We also found that language is a vital consideration in collaborations. This could pose a challenge to collaboration, as language barriers may impede communication and limit the flow of information. Future research could investigate the impact of language on collaborations and identify strategies to overcome language barriers to facilitate collaborations across borders [40].

The United States is the most prolific contributor to Y90 radioembolization research, with a high number of authored articles and overall citation count. The strong academic focus of the USA can be attributed to the country's well-funded institutions and renowned universities [44].

Collaboration among authors, particularly those affiliated with Northwestern University, highlights the importance of establishing strong professional connections and working together on research projects in the field of Y90 radioembolization. The united dedication of Salem, R., Lewandowski, R.J., Mulcahy, M.F., Sato, K.T., and Kulik, L. resulted in remarkable research output, with 16 co-authored articles [19, 33, 45], receiving a total of 2030 citations (excluding self-citations). The authors' strong collaboration ties and high link strength emphasize the significance of promoting intra-institutional collaboration to facilitate high-impact research.

Encouraging collaboration among researchers, both within and across institutions, could lead to groundbreaking findings, driving innovation and advancements in the field of Y90 radioembolization. The significant positive correlation between the number of links and published articles highlights the critical role of collaboration in increasing research output, making this finding valuable for researchers seeking to maximize their impact and contribute effectively to their field.

Conclusions

In conclusion, this comprehensive bibliometric analysis of the top 100 cited articles in Yttrium-90 Radioembolization (Y90) research provides critical insights into the evolution, advancement, and influence of research within this domain. Key findings indicate that most impactful studies have been published in high-impact journals, with significant contributions from leading institutions like Northwestern University. Despite no significant correlation between journal impact factors and citation metrics, the clustering of citations in specific journals highlights the need for strategic targeting when disseminating research outputs. Additionally, the correlation between collaborative links and publication productivity underscores the importance of collaboration in driving impactful research. These insights are not only vital for researchers and institutions in aligning their efforts towards impactful studies but also for policymakers and funders in prioritizing support for areas yielding high collaboration and citation impacts. Thus, the study aids in refining strategies for future research directions, funding allocations, and institutional collaborations, ultimately enhancing the application and understanding of Y90 treatments in clinical settings.

Limitations

Bibliometric analyses face accuracy and reliability limitations due to factors such as temporal bias, citation lag, self-citation, preferential citation practices, and citation cartels, which can influence article rankings. The study's focus on the Web of Science database, which prioritizes English publications, may introduce biases. Finally, although the study acknowledges language's role in collaboration patterns, the study does not explore strategies for facilitating cross-border collaborations or address inherent limitations, which could be a focus for future research.

Availability data and materials

The dataset(s) supporting the conclusions of this article is(are) is available in data repositories.

Abbreviations

Y90:

Yttrium-90 radioembolisation

TARE:

Trans-arterial radioembolization

HCC:

Hepatocellular carcinoma

ICC:

Intrahepatic cholangiocarcinoma

JVIR:

Journal of vascular and interventional radiology

IQR:

Interquartile range

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Acknowledgements

The authors declare that they had full access to all of the data in this study and the authors take complete responsibility for the integrity of the data and the accuracy of the data analysis.

Funding

No funding was received for this study.

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Authors and Affiliations

  1. Department of , of Medicine, University of Galway, University Road, Galway, Radiology, School H91TK33, Ireland

    Hassan Mahmood & Avinash Deshwal

  2. Fiona Stanley Hospital, 11 Robin Warren Dr, Murdoch, WA, 6150, USA

    Avinash Deshwal

  3. School of Medicine, University College Dublin (UCD), Belfield, Dublin 4, Ireland

    Aleena Khalid & Ethel Mc Manus

  4. Galway, H91 WVK3, Ireland

    Hassan Mahmood

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  1. Hassan Mahmood
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  2. Avinash Deshwal
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  3. Aleena Khalid
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  4. Ethel Mc Manus
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Contributions

Hassan Mahmood: Conceptualisation, Methodology, Software, Formal analysis, Investigation, Writing—Original Draft, Visualisation, Supervision. Avinash Deshwal: Validation, Investigation, Writing—Review & Editing. Aleena Khalid: Software, Formal analysis, Visualisation. Ethel Mc Manus: Validation, Investigation, Writing—Review & Editing.

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Correspondence to Hassan Mahmood.

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No ethics approval was required as this was a bibliometric study based on previously published literature. No subjects were involved in the study this no consent was required.

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Mahmood, H., Deshwal, A., Khalid, A. et al. Mapping the landscape of Y90 radioembolisation research: a citation analysis of the top 100 papers. Egypt J Radiol Nucl Med 55, 169 (2024). https://doi.org/10.1186/s43055-024-01339-3

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