Over the years, orthopaedic surgery has witnessed remarkable advancements, including the emergence of new, groundbreaking fields such as orthopaedic oncology. This subspecialty focuses on the treatment of primary benign and malignant lesions as well as metastatic bone and soft-tissue tumors. Despite notable progress, there is still an underexplored aspect in the realm of orthopaedic oncology: the comprehensive understanding of the scientific landscape, including pivotal articles that have shaped and influenced the field.1

Assessing the true impact of individual studies is challenging. Only through the passage of time, we can accurately gauge whether a study provides an important perspective, a new claim, or a breakthrough observation. Citation count is a simple, yet reliable, metric to quantify the frequency with which a study has been credited by peers and, indirectly, attribute relevance to the work. A bibliometric analysis relies on this metric that highlight past and current trends and trace the overall development of a scientific discipline over time.2 Furthermore, assessment of the most cited studies can provide additional insight on widely acknowledged topics such as the underrepresentation of women in surgical specialties, particularly in orthopaedics.3,4

Bibliometric analyses have been conducted in different realms of orthopaedics such as pediatrics,5 arthroplasty,6 and general orthopaedics.7,8 In orthopaedic oncology, only one study described the most frequently cited papers within the field.1 However, this study only described the 50 top-cited studies and failed to conduct an analysis on more granular details such as study type or topic. We conducted an in-depth analysis of the 500 most cited papers in the field of orthopaedic oncology and sought to answer the following questions: (1) What are the main demographic and bibliometric characteristics of the 500 most cited studies in orthopaedic oncology? (2) How has female involvement as either first or senior authors evolved over the past 60 years? (3) What were the most cited topics and trends in orthopaedic oncology across the past 6 decades?

Methods Search Strategy

The Science Citation Index Expanded database of the Web of Science (WOS) Core Collection database was used to find the most cited articles. On May 12, 2023, we conducted a search of the WOS database for articles published in any of the 223 journals in the WOS category “Orthopedics.” Our search resulted in 452,288 results, which were further filtered by the subtopic titled “Soft Tissue, Bone, & Nerve Cancers” and yielded 14,920 studies published between 1965 and 2023. Among these, we selected the 500 articles with the highest accumulated citation count. All articles were available in the English language. Their full citation and citation count are given in Supplementary Table 1, https://links.lww.com/JG9/A315.

Data Extraction

All 500 articles selected were manually reviewed, and qualitative and quantitative data were extracted into a standardized sheet. The following variables were extracted: name of the first and senior author (both full name and name in citation format), sex of the first and senior author, author count, year and decade of publication, manuscript name, institution and country where the study was done, journal where the study was published, type of study (single vs. multi-institutional), study design, and study topic. Affiliations in England, Scotland, Northern Ireland, and Wales were reclassified as being from the United Kingdom (UK).9

Author sex was obtained by looking up the author's name and matching it based on institution and year. When the author could not be identified, as was the case with many first authors, the Genderize database (www.genderize.io) was used. The Genderize database contains more than 200,000 across 79 countries and 89 languages, and its algorithm assigns a gender probability by associating the name provided with their database.10 Based on previous orthopaedic literature, a 90% probability threshold was applied to the results of the gender assignment.4,11

The following study designs were established before the start of the study: (1) case report/case series, (2) cohort study, (3) controlled trial, (4) review (narrative or systematic), (5) preclinical/basic science study, (6) big database study, and (7) development/implementation of questionnaires or scores. Distinction between case series and cohort studies was based on the guidelines established by Dekkers et al.12

Statistical Analysis

Total and yearly citations were the main metrics analyzed. Yearly citation was calculated by dividing the citation count of each manuscript by the number of years that have passed since publication. Continuous variables were displayed as means ± SD, and simple proportions (rates) were calculated for categorical values. The chi-square test was used to compare differences between categorical values. The T-test was used to compare mean values of continuous variables. A P value ≤ 0.05 was considered statistically significant. All analyses were done using StataSE 14 (StataCorp).

Results What Are the Main Characteristics of the 500 Most Cited Studies in Orthopaedic Oncology?

The top paper, “A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system”—Enneking 199313 was cited 1808 times, and the bottom 15 papers were each tied for citations at 81. The mean number of citations was 147. The oldest article was published by Chung et al14 in 1965 with 103 citations, and the most recent in 2018 by Misaghi et al15 with 242 citations. The most frequently published author as either first or senior author was Mankin HJ, followed by Enneking WF and Sim FH (Table 1).

Table 1 - Authors Who Published the Most Cited Papers Author Count Mankin JH 29 Enneking WF 17 Sim FH 16 Campanacci M 14 Grimer RJ 10 Simon MA 9 Marcove RC 7 Dahlin DC 7 Healey JH 7

Most articles from our list originated from nine countries. We found the United States to be the leading publishing country (53.6%), followed by the United Kingdom and Italy (Table 2). Fourteen percent of articles originated from non-English speaking countries. Among institutions, the Mayo Clinic led in the number of published articles (45, 6590 citations), followed by the Royal Orthopaedic Hospital (32) and the Massachusetts General Hospital (30). The University of Florida at Gainesville was ranked sixth in article count yet had the highest total citation count (6,930) (Table 3).

Table 2 - Countries of Origin of the Most Cited Papers Country N (%) Total Citations Yearly Citationsa United States 254 (53.6%) 42,334 5.83 ± 6.94 United Kingdom 40 (8.4%) 5,030 6.63 ± 3.71 Italy 36 (7.6%) 5,316 7.17 ± 5.56 Germany 21 (4.4%) 2,874 7 ± 3.92 Japan 20 (4.2%) 2,235 4.55 ± 2.28 Canada 18 (3.8%) 2,556 6.11 ± 2.95 Sweden 11 (2.3%) 1,615 3.91 ± 2.17 China 8 (1.7%) 900 9.75 ± 5.39 Argentina 7 (1.5%) 847 4.86 ± 3.02

aValues displayed refer to mean ± SD.

Table 3 - Institutions Most Represented in Top-cited Papers Institution N (%) Total citations Yearly citationsa Mayo Clinic 45 (9.7%) 6,590 4.51 ± 3.5 Royal Orthopaedic Hospital 32 (6.9%) 4,234 7.34 ± 3.69 Massachusetts General Hospital 30 (6.5%) 5,865 6.9 ± 4.4 Istituto Ortopedico Rizzoli 19 (4.1%) 2,853 7 ± 5.87 University of Florida, Gainesville 17 (3.7%) 6,930 12 ± 14.3 Memorial Sloan Kettering Cancer Center 16 (3.4%) 2,300 3.56 ± 2.31 Italian Hospital of Buenos Aires 6 (1.3%) 682 5.17 ± 3.19 University of California, Los Angeles 6 (1.3%) 653 4.17 ± 4.83 Columbia-Presbyterian Medical Center 5 (1.1%) 683 2 ± 1

aValues displayed refer to mean ± SD.

The articles were published across 29 different journals, with the most common being the Journal of Bone and Joint Surgery American Volume, followed by Clinical Orthopaedics and Related Research and the Bone & Joint Journal (formerly known as Journal of Bone and Joint Surgery British Volume) (Table 4). The journals with the highest mean yearly citation count were Orthopaedic Clinics of North America (10.1) and Clinical Orthopaedics and Related Research (6.38).

Table 4 - Journals With the Most Cited papers Journal N Total Citations Yearly Citationsa IF Journal of Bone and Joint Surgery (Am) 166 (33.2%) 29,627 5.4 ± 4.8 5.3 Clinical Orthopaedics and Related Research 112 (22.4%) 17,104 6.38 ± 6.7 4.2 Bone & Joint Journal b 76 (15.2%) 9,485 5.45 ± 3.76 3.31 Skeletal Radiology 42 (8.4%) 4,539 4.62 ± 2.45 2.1 Spine 25 (5.0%) 3,213 5.52 ± 3.4 3 Acta Orthopaedica Scandinavica 14 (2.8%) 1,889 3.71 ± 1.49 1.02 Orthopaedic Clinics of North America 10 (2.0%) 1,500 10.1 ± 16.1 0.9

IF = impact factor

aValues displayed refer to mean (SD).

bFormerly known as Journal of Bone and Joint Surgery–British Volume.

Most articles were cohort studies (73.2%), 9.2% were reviews, and 6.8% were case reports (Table 5). The decade of the 2000s produced the greatest number of articles, followed by the 1990s and 1980s. Most articles were done at a single institution (81.7%). The median number of authors per article was 4.

Table 5 - Characteristics of Included Studies Variables N (%) Study design  Case report 34 (6.8)  Cohort study 366 (73.2)  Randomized controlled trial 6 (1.2)  Review (narrative or systematic) 46 (9.2)  Preclinical study 33 (6.6)  Large database study 3 (0.6)  Questionnaire/score development 5 (1.0)  Other 7 (1.4) Publication decade  1960s 18 (3.6)  1970s 51 (10.2)  1980s 85 (17.0)  1990s 135 (27.0)  2000s 170 (34.0)  2010s 41 (8.2) Study type  Single institution 406 (81.7)  Multi-institution 91 (18.3) Author number per articlea 4 (3-6)

aValue displayed refers to median and interquartile range between brackets.

How Has Female Involvement as Either First or Senior Authors Evolved Over the Past 60 Years?

The frequency of male authors in both first and senior positions was higher across all decades in comparison with the number of female authors. Female involvement in first author positions significantly grew from zero in the 1960s to 14.6% in the 2010s (P = 0.0434). However, no statistically significant difference was observed when comparing the frequency of female first authors decade-to-decade (Figure 1, A). Similarly, female participation as senior authors increased from no participation in the 1960s to 12.2% in the 2010s decade (P = 0.0607) (Figure 1, B).

Figure 1:

Graph showing the gender distribution in the orthopaedic oncology literature as (A) first authors or (B) senior authors.

What Were the Most Cited Topics and Trends in Orthopaedic Oncology Across the Past 6 Decades?

We determined the most common orthopaedic oncology topics from articles published in each decade. For studies published in the 1960s, pigmented villonodular synovitis was the most cited topic (Figure 2). Studies focusing on primary bone sarcomas were the most common in the 1970s and 1980s (21.6% and 14.1%, respectively). Bone cysts were the third most cited topic consistently from studies published from the 1970s to the 1990s. Citations for studies performed from the 1990s up until the 2010s were more commonly done for the subject of reconstruction procedures. Giant cell tumor of bone was the third most cited topic from the 2000s, and the second most cited from studies published in the 2010s.

Figure 2:

Graph showing the most common orthopaedic oncology topics by publication decade.

Discussion What Are the Main Characteristics of the 500 Most Cited Studies in Orthopaedic Oncology?

We conducted an analysis of the 500 most cited papers in the field to gain insight into the history and development of this subspecialty in orthopaedic oncology. Our study revealed a progressive increase in the number of highly cited articles since the 1960s, indicating a growing field. Although over a third of the papers on our list were published in the 2000s, the top 10% of cited papers contained only 15 from this decade or beyond. This can be logically attributed to the longer time that older articles have been around, providing them with more time to acquire citations. Our review of these articles identified several landmark studies within orthopaedic oncology, including the first and second most cited papers: “A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system”13 and “A system for the Surgical Staging of Musculoskeletal Sarcoma,”16 both by Enneking et al. In the first article, the authors developed the first system to assess functional outcomes in both upper and lower limbs after tumor resection, while the second study provided a novel classification of tumor stage that paved the way for the adequate management of bone and soft-tissue sarcomas. We found that most of the papers in our list were made in the United States (53%), which is comparable with other specialties such as anesthesiology (69%), critical care (69%), and general surgery (63%).17–19

How Has Female Involvement as Either First or Senior Authors Evolved Over the Past 60 Years?

Gender inequality in orthopaedic surgery has been previously assessed,4,20–23 yet information in orthopaedic oncology is limited. Our study showed that there is a notable disparity in the frequency of men and female authors, both as first and senior authors, among the most cited articles. However, this difference has improved over time. Over the past 6 decades, we found an important increase in women in both first and senior authorship positions. A similar trend regarding female first authorship has been reported in other subspecialties such as foot and ankle, spine, sports medicine, and hand surgery.3,11,24,25 Despite this, there is also evidence that the percentage of women in senior authorship positions has decreased in other fields, particularly between the 2000s and the 2010s.4,24 Xu et al reported in 2020 that the proportion of female senior authors in arthroplasty research decreased from 8.5% to 6.2% from 2002 to 2019. Similarly, Vora et al found that although there had been progression in female senior authorship in foot and ankle surgery between 1993 and 2008 (0% vs 15.4%), by 2017, this percentage had dropped to 13.5%. Because first authors are commonly trainees, the increase in their prevalence will hopefully result in an increase in senior authors in the future. Overall, our results show that although there are still differences between male and female proportions in these positions, progress is being made in our field regarding gender diversity. This could be a result of the difference in gender composition across the field getting smaller. For example, the proportion of female orthopaedic surgery residents in the United States increased from 9.8% in 2004 to 2005 to 15.4% in 2019,26 and 19% in a more recent study assessing the 2017 to 2021 period.27 However, notably, these numbers are low compared with other specialties. In the 2016 to 2017 period, only 14% of all orthopaedic surgery residents were women, the lowest percentage across all specialties in that period.28 These findings underscore the point that although female participation in orthopaedic training is growing, it is doing so very slowly. Because of this, we need to continue supporting women and apply mitigating strategies to problems such as gender bias and sexual discrimination, which are known to still exist.26,29 These mitigating strategies should include encouraging women to apply to orthopaedic surgery residency, provide adequate research training, and empower them to take on leadership roles.

What Were the Most Cited Topics and Trends in Orthopaedic Oncology Across the Past 6 Decades?

Although the most common topic of the 1960s was pigmented villonodular synovitis, the three articles with the highest citation count in the period focused on osteosarcoma and unicameral bone cysts.30–32 This includes a cohort of Dahlin et al of 600 patients with osteosarcoma, the paper by McKenna et al on the histogenetic origin of osteogenic sarcoma, and Neer's cohort of unicameral bone cysts in which he established a healing grading system based on radiological changes of the lesion over time. This system is still being used today, albeit with modifications.33 In our list, a total of 51 articles were published in the 1970s, and 85 in the 1980s, with primary bone sarcomas being the most cited topic from articles produced in both decades. Interestingly, in the 1970s, osteoid osteoma and osteoblastoma ranked second, while in the 1980s, giant cell tumor of bone took the second spot. This could be attributed to the significant impact of the article by Goldenberg et al34 on giant cell tumor of bone, which was published in 1970 and is now the fourth most cited paper on our list. Another noteworthy contribution was made by Campanacci et al in 1987, whose cohort study on the same topic became the third most cited paper in our list.35 This topic has remained persistently studied, being the third most cited topic in the 2000s and the second most cited in the 2010s. The topic of reconstruction procedures began to emerge in the late 1970s and has since become the predominant topic in orthopaedic oncology literature. The most cited paper on this topic is “Resection and Reconstruction for Primary Neoplasms Involving the Innominate bone” by Enneking et al in which he demonstrated that wide excision was an acceptable method of treatment in select cases, therein creating an alternative to the more popular hemipelvectomy which carried concomitant functional and psychological disabilities.36 These studies began to emphasize surgical techniques over clinical and pathological descriptions of diseases, and the popularity of this topic increased with the development of new reconstruction techniques, including biologic and prosthetic reconstructions. This movement toward innovative techniques was further pushed by advancements in other medical technology. Chemotherapy and radiation therapy saw rising success in the treatment of osteosarcomas, which allowed for more patients to be considered for limb-salvaging procedures rather than amputations.37

Our study presented several limitations. First, because we analyzed articles based on citation count, we were limited in our capacity to analyze more recent trends in our field. As technology develops, new areas of research are created every day. For instance, the exponential surge in interest surrounding robot-assisted surgery38 and 3D printing39 has markedly increased the annual number of publications since 2014. There is also an imminent integration of artificial intelligence and machine learning in the field's future. All these technological advancements have the potential to reshape the landscape of our subspecialty and enhance the quality of life for patients with orthopaedic oncology. Second, the use of the WOS Journal Citation Report could be a limitation as well. The reliance on citation indexes to gauge study relevance and impact has been questioned before.40 Technical limitations may result in the inadvertent omission of certain papers from our analysis. Nonetheless, our study presents several strengths. A previous bibliometric analysis on orthopaedic oncology was made in 2018.1 However, this article only included the 50 most cited articles in the field, which we consider inadequate to comprehensively analyze the trends on this subspecialty. Moreover, our study conducted an in-depth manual review of all included studies to see patterns in gender publication rates and research topics across time.

This comprehensive analysis provides a comprehensive picture of the development of orthopaedic oncology. We have entered an era in this field characterized by an emphasis of research on surgical techniques and its role in the well-rounded management of these patients. Notable progress has also been made in gender diversity over the past 6 decades, with more women contributing as first and senior authors in orthopaedic oncology research. However, disparities still exist, and the field should continue efforts to promote gender equality. As the landscape continues to evolve, it remains crucial to maintain the momentum toward inclusivity, innovation, and collaboration to further advance orthopaedic oncology for the betterment of patient care and medical progress.

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