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Orthopedic approaches for bone sarcoma: A bibliometric review of the 50 most cited papers
, Zachary Donatoa, David S. Constantinescub, Waleed Al-Hardanb, Max Barona, Brooke Crawfordb
∗Corresponding author: Moses I. Markowitz. Moses.markowitz@med.miami.edu
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Received: ,
Accepted: ,
This article was originally published by Reed Elsevier India Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.
Abstract
Abstract
Curative treatment of bone sarcoma is primarily based on operative management. The Orthopedic Oncology approach towards this disease has evolved greatly to the breakthrough in systemic treatment options as well as unique implant designs favoring limb salvage over amputations. The purpose of this study was to perform a bibliometric analysis of the top 50 most cited papers related to the orthopedic the approach to bone sarcomas.
We queried the ISI Web of Knowledge database in July 2022. Keywords utilized were: ““Bone Sarcoma” OR “Osteosarcoma” OR “Ewing Sarcoma” OR “Chondrosarcoma” OR “Chordoma”. The top 50 articles pertaining to the orthopedic approach to bone sarcoma were included for analysis and included manuscript title, authors, citation count, journal and publication year.
The mean number of citations are 187.06 (Range 125–400; SD 67.83). The average citations per year is 10.03 (Range 47.86–3.43; SD 8.05). Many articles were published from 2000 to 2009 (n = 20) and 1990–1999 (n = 13). The majority of the articles were published by institutions within the United States (n = 32). The most common level of evidence was level IV (n = 37). Majority of the articles focused on treatment outcome (n = 22).
This study offers a comprehensive review of the most cited literature regarding orthopedic approaches to bony sarcomas. Modern treatment approaches for bone sarcoma has resulted in an increased focus within the literature on achieving disease free survival wide tissue margins. Understanding the trends of available studies allows for physicians and researchers to target and innovate future areas of study.
1 Introduction
The modern treatment of bone sarcoma is a success on many fronts. Patients are now treated with operations that significantly improve postoperative function. The treatment approach of these tumors has evolved significantly, combining systemic chemotherapy with a curative orthopedic procedure.1 These sarcomas, however, demand wide local resection in order to obtain negative margins and thus pose a unique problem for an orthopedic oncologist in certain anatomic locations.2 When considering all of the literature related to the orthopedic approach to bone sarcoma, some articles were highly influential to the development of the modern approach to bone sarcoma.
Although the true impact of a scientific paper cannot be quantified, its influence can be inferred from the number of times it has been cited. A list of the most frequently cited papers on a given subject shows particular trends in the most important papers and reveals the scientific community's focus on the topic. This, termed a bibliometric analysis, has been conducted in other fields and procedures within orthopedics.3–6 It has recently been performed assessing the most cited articles pertaining to orthopedic oncology.6 However, despite the significant attention that bone sarcomas have received in orthopedic oncology, an analysis of the most frequently cited papers pertaining to these tumors has not been yet been performed. The objective of this review is to conduct a bibliometric analysis to assess the top 50 papers related to orthopedic oncology procedures for bone sarcoma.
2 Materials and methods
In July 2022, we searched the ISI Web of Knowledge database to identify articles related to bone sarcoma. The following keywords were utilized for the search: “Bone Sarcoma” OR “osteosarcoma” OR “Ewing Sarcoma” OR “chondrosarcoma” OR “chordoma”. Journals categorized in the “Orthopedics” and “Surgery” category cover all clinical and basic science journals with direct and peripheral relations to each respective field. To better evaluate the most popular articles about orthopedic procedures for bone sarcoma, all included articles were limited to these categories.
The search covered all articles that had undergone peer review. The search was not limited by article type, language, level of evidence, or date of publication. The articles were then arranged in order of greatest to least total citations. Then, all articles were reviewed by two independent researchers who screened each article by their title and abstract, excluding any that were unrelated to orthopedic procedures for bone sarcoma.
3 Results
The search yielded 45,923 results. This was then filtered to articles within the “Surgery” or “Orthopedics” categories, reducing the list to 6919 articles. These articles were then ranked in descending order of total citations. 91 articles were subsequently excluded as they did not pertain to orthopedic procedures for bone sarcoma. The top 70 articles were assessed further, of which the 20 with the fewest citations were excluded. This yielded the top 50 most cited articles pertaining to orthopedic procedures for bone sarcoma (Fig. 1).
The top 50 articles are listed in Appendix. The mean number of citations is 187.06 (Range 125–400; SD 67.83). The average citations per year is 10.03 (Range 47.86–3.43; SD 8.05). All articles were published from 1956 to 2018, with the greatest portion of articles published from 2000 to 2009 (n = 20) (Fig. 2).
The top 50 articles were contributed by a total of 16 distinct journals. The most articles (n = 19) came from the Journal of Bone and Joint Surgery - American Volume, which was followed by Clinical Orthopaedics and Related Research (n = 6), and Spine (n = 6) (Fig. 3). The majority of the articles were published associated with institutions within the United States (n = 32), followed by Italy (n = 7), Sweden (n = 3), and England (n = 2). Canada, China, Germany, Israel, Japan, and Norway all contributed 1 article each to the top 50 list (Fig. 4). Several institutions contributed multiple articles to the list (Fig. 5). Of the top 50 articles, Mayo Clinic (n = 6) contributed the most, followed by Instituto Ortopedico Rizzoli (n = 5), Massachusetts General Hospital (n = 5), University of Miami Miller School of Medicine (n = 2), and the University of Minnesota Cancer Center (n = 2).
The most common level of evidence was level IV (n = 37), followed by II (n = 5), V (n = 5), III (n = 2), and I (n = 1). Many of the articles focused on treatment outcome (n = 22), followed by prognostic indicators and epidemiology (n = 12), natural history (n = 9), surgical technique (n = 5), and classification (n = 2). There were no articles in the top 50 that focused on clinical guidelines or anatomy and biomechanics. Of the articles focused on treatment outcome, 59.1% (n = 13) discussed the importance of adequate resection and wide surgical margins. Many of the articles focused only on osteosarcoma (n = 13), followed by chondrosarcoma (n = 11), chordoma (n = 9), and Ewing Sarcoma (n = 2). However, the greatest portion of the top articles focused on multiple types of bone sarcoma (n = 15) (Fig. 6). Furthermore, a significant number of the articles (n = 12) concentrated on spine tumors specifically.
4 Discussion
In this review, the top 50 most-cited articles related to orthopedic procedures for bone sarcoma were identified systematically and analyzed. These articles assessed treatment outcomes, prognostic indicators and epidemiology, natural history, surgical techniques, and classifications related to bone sarcoma. In our analysis, most articles focused on treatment and outcomes. Of these articles, the majority assessed the importance of wide surgical margins and adequate resection on patient survival and rate of recurrence of these tumors. This is the forefront of surgical management of bone sarcomas and is fitting to be the focus of the most influential publications. Adequate margins of excision are strongly associated with the risk of recurrence.7,8 Many influential articles conclude that aggressive surgical resection is indicated in patients with osteosarcoma, Ewing Sarcoma, chondrosarcoma, and chordoma.9–12 A focus in the literature on the necessity of a radical surgical approach is highlighted by the increased citations in these topics. Furthermore, many of these important articles (24%) concentrated specifically on tumors involving the spine. This demonstrates that the literature has an increased focus on articles discussing management of a region in which wide local excision can be problematic.
The majority of the papers were published after 1990 (80%) and 20 articles alone were published in the years 2000–2010. This increased influence of articles during those years is due to the recent advances in treatment of bone sarcoma. Randomized clinical trials in the late 1980s demonstrated significant increases in survival with the addition of combinations of different chemotherapy agents.13–16 After significant increases in survival were proven, orthopedic oncology surgeons began to focus their interests in opportunities for limb salvage in these patients. Treatment with neoadjuvant chemotherapy followed by salvage procedures provided patients with a curative solution while preserving function.17,18 Following the development of this innovative treatment approach, numerous articles were published soon after which evaluated its outcomes. These articles had a significant impact within the scientific community.
The three most cited articles were published in the Journal of Bone and Joint Surgery – American Volume. The most cited paper, by Simon et al., was a comprehensive longitudinal investigation spanning 26 institutions that examined functional outcome, morbidity, and quality of life for patients who received an above the knee-amputation, a limb salvage procedure or disarticulation of the hip.19 Oncological follow up data, functional outcomes, and quality of life were all assessed. The results of this study showed that survival rates or disease-free survival rates did not significantly differ between the groups. Furthermore, in comparison to the other two types of amputations, limb salvage operations were associated with a significantly higher rate of reoperation. Functional outcomes, using the modified Tumor Society Score, were significantly higher for the limb-salvage group compared to either the above the knee amputation or disarticulation of the hip groups. This multi-institution study demonstrated that limb salvage procedures demonstrate similar survival rates when compared to amputation yet resulting in a significantly improved functional outcome.
The vast majority of the articles within the top 50 had a low level of evidence, with 95% (n = 43) of the articles being level of evidence IV or V. This identifies a paucity within the most influential articles of high level of evidence studies. Though multiple randomized controlled trials exist assessing chemotherapy regimens as adjuncts to surgical management,13–16 these studies were not as frequently cited as other papers analyzing the results of the combination treatment approach. This indicates that other study designs, such as database analyses and retrospective cohorts, were cited more than randomized controlled trials despite having a lower level of evidence.
The countries that contributed the top 50 articles, similarly to other bibliometric analyses within orthopedic oncology, were comprised mainly of institutions within the United States.6 Just as the bibliometric analysis by Cevik et al. that assessed the top 50 papers within orthopedic oncology, Italy, specifically Instituto Ortopedico Rizzoli, contributed a large portion of the most cited articles.6 This institution contributed more articles alone than any single other country outside of the United States.
When comparing articles studying each type of bone sarcoma, osteosarcoma was the focus of most of the articles (n = 13). It is understandable that articles focusing on the orthopedic approach to this tumor are heavily cited, as osteosarcoma is the most prevalent malignant bone neoplasm (36%).20 There was also a significant portion of the top 50 most cited articles focused on chondrosarcoma (n = 11), while only two articles investigated Ewing Sarcoma. Many articles, however, discussed multiple bone sarcomas generally (n = 15), focusing on the implications of surgical treatment on metastasis and recurrence (Fig. 6).
4.1 Osteosarcoma
There is no surprise that osteosarcoma has been heavily investigated given the huge advancements in prognosis over the past few years.21 In a heavily cited review “Update on Survival in Osteosarcoma” published in 2016, Anderson et al. elegantly address the successes in treatment for osteosarcoma over the last decade.21 A disease once rarely curable has now reached almost a 70–80% five-year overall survival rate. This paper discusses several prognostic factors including current survival prediction based on metastatic disease, chemotherapy response, tumor characteristics, and patient characteristics. Developments in chemotherapy regimens again have fallen short over the past decades, leading to a plateau in survival for patients with localized disease.21 One more promising treatment focuses on using the immune modulator L-MTP, with initial studies noting an 8% increase in survival at six years and the importance of targeted immunotherapy based on specific molecular markers.22,23 Another 2016 study by Mason et al. demonstrates that molecular targeting of HER2 signaling pathways have been shown in some studies to reduce metastatic disease.24
4.2 Ewing Sarcoma
Ewing sarcoma is the second most common primary bone malignancy in children and adolescents,25 and since the introduction of chemotherapy, prognosis has been much more favorable especially in localized tumors.10,25 In a heavily cited retrospective cohort study, Wunder et al. (1998) elucidate how the response to neoadjuvant therapy may predict prognosis.10 The study included a sample size of 74 patients with Ewing Sarcoma treated with both preoperative and postoperative chemotherapy with resection and radiation in some patients. In the study, the histological response to chemotherapy was found to be the most important factor in disease-free survival in patients without metastatic disease and with metastatic disease without bone marrow involvement. Prognosis was not, however, associated with the initial presence or absence of metastases.10 Ultimately, Wunder et al. provided a framework for future management in identifying patients that are high risk for metastases that may warrant a more intensive treatment approach.
4.3 Chondrosarcoma
Chondrosarcoma is a rare primary bone tumor, and therefore much of what has been presented in the data have been through case reports and case series.26 In 2009, Giufridda et al. provided a much larger study, “Chondrosarcoma in the United States (1973–2003): An Analysis of 2890 Cases from the SEER Database”.26 This study used the SEER database, a validated national epidemiological surveillance system to identify demographic and prognostic information on 2890 patients diagnosed with chondrosarcoma. Results show that female sex, histological stage, and surgical stage were associated with a significant survival benefit.26 Additionally, those patients who survived for more than ten years were more likely to die of conditions unrelated to chondrosarcoma.26 This study was valuable in assessing survival based on histologic subtype of the tumor. Another influential study by Fiorenza et al. in chondrosarcoma, “Risk factors for survival and local control in chondrosarcoma of bone” published in 2002, studied 153 patients and investigated the various factors contributing to localized tumor control in non-metastatic disease.11 The study demonstrates, with multivariate regression, that recurrence is associated with worse survival rates. In addition, extra-compartmental spread was significantly correlated with inadequate margins, local recurrence, and poor survival. The authors specifically point to the difference in survival rates for stage 2B tumors without local recurrence compared to those with recurrence (64% vs 4% survival rate, respectively).11 This highlights the importance of ensuring adequate margins for the treatment of chondrosarcoma.
4.4 Metastatic bone sarcoma
Many of the top cited papers on bone metastases have been written about osteosarcoma. Local therapy alone is not an effective treatment for osteosarcoma because over 80–90% of patients with seemingly localized malignancy will develop metastases.27 This is based off the principle that even patients without clinically detectable metastases are assumed to have micrometastases present. In high grade osteosarcomas, the primary goal of preoperative chemotherapy is to treat detectable metastases or presumed micrometastases, as well as a neoadjuvant role to potentially shrink the size of the primary tumor.28
In cases that are deemed eligible for surgical management, the current surgical approach to metastatic osteosarcoma involves local tumor resection with a possible additional surgery to remove all known metastatic foci. This was assessed in a 2003 study by Kager et al. (2003), demonstrating that in patients treated with this surgical approach, there is approximately a 30% long-term survival rate.29 Additionally, in patients with nonmetastatic osteosarcoma of the extremity, metastatic disease recurs in 30% of patients despite complete surgical removal with negative margins and an intensive chemotherapeutic regimen.30–32 It is estimated that 90% of these relapses are due to lung metastases.33 Briccoli et al. published an influential cohort study in 2009 on high grade osteosarcoma of the extremities metastatic to the lung after treatment with thoracotomy for resection of tumor metastases.34 In the cohort, the five-year overall survival rate was 37%. Additionally, this survival rate was positively correlated with an increased relapse interval, finding that the best prognosis was for patients with relapse after 24 months.34 In a 2010 review study, Ritter et al. demonstrates that thoracotomy should always be performed when complete removal of metastatic foci is reasonable.27 It also indicates that there is a lack of evidence regarding salvage chemotherapy to be beneficial, noting that chemotherapy regimens consist of the same drugs that were used in the 1980s, including doxorubicin, cisplatin, methotrexate, and ifosfamide.27 Ritter et al. emphasize the importance of investigating innovative therapies with multicenter efforts. They discuss the potential role of immunomodulation, citing one study where the addition of muramyl tripeptide phosphatidyl ethanolamine (MTP), to postoperative chemotherapy was correlated with a statistically significant difference in survival rate.23
Most years, the Journal of Bone and Joint Surgery publishes an article titled “What's new in musculoskeletal tumor surgery”, most recently published in 2022. This extensive and important review, authored by Gazendam et al., even discussed the recent advances in metastatic bone sarcoma.35 Related to osteosarcoma, this paper discusses updates in survival for motile vertebral column sarcomas. When comparing five-year overall survival between osteosarcoma and other forms of sarcoma, osteosarcoma has the worst prognosis.35 The “What's new in musculoskeletal tumor surgery” from 2021 also contained important updates regarding osteosarcoma.36 This article discussed a study by Gusho et al. (2021), which reported on the outcomes of lymphovascular invasion in localized osteosarcoma at a single institution over a ten-year period.37 This retrospective study of high-grade localized osteosarcoma identified important prognostic and mortality data. Lymphovascular invasion was found to be present in 21% of cases and was associated with a very poor prognosis (20% survival rate at ten years).37 Pertaining to Ewing Sarcoma, one retrospective study by Stachelek et al. (2021) assessed a series of patients with localized non-metastatic disease over a twenty-year period and tabulated predictors of recurrence.38 Importantly, they found that poor responses to neoadjuvant chemotherapy and certain tumor characteristics, such as tumor necrosis <95% following neoadjuvant chemotherapy, were significant predictors of recurrence in localized disease.38 In chondrosarcoma, Laitinen et al. (2022) compared oncologic outcomes between centrally and peripherally located tumors.39 This study of 714 patients revealed equal disease-specific survival amongst the different subtypes after controlling for tumor grade.39 Local recurrence-free survival was also similar for different locations and subtypes after adjustment for surgical margin.39 This highlights the importance of considering tumor grade and disease-free margins for chondrosarcoma, while demonstrating that other factors are not necessarily predictive of recurrence or survival for this disease.
There are limitations to this study. It is impossible to determine a scientific article's true impact. Although ranking articles by their total number of citations is one way to gauge their importance, other noteworthy articles with lower total citation counts might have been left off of this list. Furthermore, by using Thomson ISI Web of Science®, it is possible that some articles that are not in this database were excluded from our analysis. Finally, in an effort to focus on the orthopedic oncology approach to bone sarcoma, we specifically examined articles within the orthopedics and surgery categories. This may have resulted in the omission of articles that are not listed in these categories.
Despite these drawbacks, our analysis of the top cited articles, assessing the orthopedic approaches for bone sarcoma research continues to be a useful mechanism for determining those articles that are most significant within this topic. This work offers a thorough overview of the caliber and content of bone sarcoma research through our examination of the level of evidence, number of citations, and demographic composition of the top 50 most cited articles. Therefore, this study can assist researchers in vetting areas for further consideration pending their specific intentions regarding bone sarcoma research.
5 Conclusions
Understanding the trends of available studies allows for physicians and researchers to target and innovate future areas of study. Modern treatment advances in bone sarcoma have resulted in an increased focus within the literature on recently published studies that discuss orthopedic procedures that achieve disease free survival with wide tissue margins. When assessing these studies, however, there is a paucity of high level of evidence studies.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Authors contribution
All authors significantly contributed to the writing of this manuscript.
Conflict of interest
The authors have no conflicts of interest to disclose.
Ethical review committee statement
This study has been performed in accordance with the ethical standards in the 1964 Declaration of Helsinki. This study was carried out in accordance with relevant regulations of the US Health Insurance Portability and Accountability Act (HIPAA).
All authors significantly contributed to the document and have reviewed the final manuscript.
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