1 Introduction

Cancer metastasis to the skeleton has a high incidence, with only lung and liver being the more common sites of secondary deposits.¹ Breast (73 %), prostate (68 %), thyroid (42 %), lung (36 %) and renal cancer (35 %) are the 5 cancers with the highest incidence of bony metastasis.² The most common primary tumour with bone metastasis is breast cancer with an incidence of 65–75 %, which carries a median survival after diagnosis of bony metastasis of 19–25 months.³ In contrast to this, primary bone tumours are relatively uncommon and account for around 0.2 % of all malignancies.⁴ The axial skeleton is the most common site of bony metastasis (80 %) with the thoracic spine being the most affected, metastasis to the bones, ribs and scull are found in 63 %, 77 % and 35 % of bony metastasis cases respectively. The humerus and femurs are affected in 53 % of cases and the remaining appendicular skeleton in only 1 %.⁵ The most common long bone affected by metastatic disease is the femur which has particular clinical significance as this is a weight-bearing bone. The majority of femoral metastases are located in the femoral neck (50 %), followed by the subtrochanteric (30 %) and intertrochanteric (20 %) regions.⁶

The incidence of patients with cancer with bone metastasis has gradually increased, along with a decrease in cancer related deaths, which has led to a sharp increase in the prevalence of bone metastatic disease, which has increased by 40 % from 2010 to 2019.⁷ Furthermore, advancements in oncological treatment of both primary and secondary tumours has led to enhanced survival. In the United States of America (USA), patients diagnosed from 2006 to 2010 had 17.4 % higher chance of surviving at least 60 months compared with 1998–2002.⁸ Subsequently, orthopaedic surgeons are increasingly consulted to review patients with the sequalae of bony metastasis, in particular, pertaining to long bones with an associated risk of fracture. Patient fitness determines the suitability for surgical treatment, which involves either resection, arthroplasty, endoprosthetic reconstruction or prophylactic fixation.⁹ In order to assist the decision making, scoring systems have been developed to provide guidance, such as the Mirels’ criteria.¹⁰ Surgical fixation of a pathological fracture of the femur due to a metastatic lesion, has been shown to have as a high failure rate as 44 % at 60 months.¹¹ Prophylactic fixation of metastatic lesions before they progress to a pathological fracture has led to improved patient outcomes.¹² Pre operative embolization can be employed to decrease perioperative blood loss, particularly in hypervascular tumours such as renal cell carcinoma metastatses.¹³

Bibliometric analyses provide an overview and objective approach to current research trends by measuring citation trends, author and institutional contributions and key topics of focus.¹⁴ These studies are valuable for determining whether there is a gap in the available research on a specific topic. For example, a previous bibliometric review by this author group identified a shortage of research on rehabilitation and postoperative management of patellar instability, despite the abundance of research on surgical techniques..¹⁵ A bibliometric analysis on surgical fixation of metastatic bone disease in 2018 found a lack of articles with high level evidence, with only 6 out of 385 studies having achieved level I or II.¹⁶ The geographical bias of high income countries publishing more highly cited articles on the topic of bony metastasis as a whole was also found during a more recent 2022 bibliometric review.¹⁷

By consolidating citation metrics, authorship and geographical patterns, our goal was to conduct an updated bibliometric analysis, to deliver an extensive overview of research related to long bone metastasis. Our aim is to assist clinicians and researchers in understanding the strengths within the body of long bone metastatic research, as well as to shape future investigations to fill gaps and improve the evidence available to steer management of an increasingly prevalent and complex issue.

2 Methods

3 Results

3.1

3.1 Citation metrics and publication trends

The top 50 articles on long bone metastatic disease, published between 1973 and 2023, were included in this analysis and can be found in appendix 1. Citation counts ranged from 16 to 1348 (median 52.5; IQR 35.5–84.25).

The most frequently cited article, with 1348 citations was published by H. Mirels in 1989, it introduced a risk stratification system for predicting pathological fracture in long bone metastatic disease and recommended prophylactic surgical fixation, when certain criteria were met.¹⁰ This is followed by Y Yazawa's retrospective study on outcomes of surgical fixation of humeral and femoral pathological fractures that was published in 1990 and has been cited 273 times.¹¹ The third most cited article with 251 citations was published in 2003 by WG Ward and focused on the surgical management of femoral metastasis¹²

Publication activity prior to the 1990s was limited, with a notable increase occurring in the early 2000s. The decade of 2000–2009 was the most productive, contributing nearly half of the top-cited studies and highlighting the growing clinical and academic focus on orthopaedic management of skeletal metastases. The citations per year is displayed in Fig. 1.

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Fig. 1 Total citations by year.

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3.2

3.2 Study designs and levels of evidence

Among the top 50 most-cited articles, retrospective cohort studies were the most common design (64 %), followed by literature reviews (26 %). No randomized controlled trials (RCTs) were identified.

According to the OCEBM framework, the distribution of evidence levels was as follows:•Level I: 0 articles (0 %)•Level II: 0 articles (0 %)•Level III: 36 articles (72 %)•Level IV: 10 articles (20 %)•Level V: 4 articles (8 %)

Fig. 2 visually represents the proportions of the levels of evidence found.

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Fig. 2 Level of evidence.

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3.3

3.3 Geographic distribution

The 50 most-cited articles on long bone metastatic disease originated from a concentrated group of regions. The United States of America (USA) was the leading contributor, accounting for 25 articles (50 %), followed by Italy (4 articles, 8 %), Canada (3 articles, 6 %), and Japan (3 articles, 6 %). Additional contributions came from France (2 articles, 4 %), the Netherlands (2 articles, 4 %), Finland (2 articles, 4 %), and South Korea (2 articles, 4 %). The United Kingdom, Germany, Denmark, Sweden, Australia, Thailand, Ireland, and South Africa each contributed a single article (2 %).

Collectively, North America and Western Europe produced more than 70 % of the included studies, underscoring their dominant role in shaping high-impact literature on metastatic long bone disease. Notably, only one article within the top 50 originated from a low- or middle-income country,¹⁰ highlighting ongoing geographic disparities in research output.

Fig. 3 depicts a choropleth world map that was generated to depict publication distribution, with darker shading representing higher output.

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Fig. 3 Choropleth map illustrating the number of publications per country.

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Collaborative authorship across international centres was evident in several high-impact articles, particularly those focused on surgical outcomes and prognostic scoring systems. Nonetheless, authorship and influence remain concentrated within a relatively limited set of regions and institutions. Although contributions were identified from the USA, Italy, Canada, Japan, France, and the Netherlands, research output continues to be dominated by North America and Western Europe.

3.4

3.4 Journals and publication sources

The 50 most cited articles on long bone metastatic disease appeared across 26 peer-reviewed journals. Table 1 and Fig. 4 demonstrate the leading journals and their respective impact factors. The leading journals by article count were:•Clinical Orthopaedics and Related Research (CORR): 14 articles (28 %)•Journal of the American Academy of Orthopaedic Surgeons: 5 articles (10 %)•Journal of Bone Oncology: 3 articles (6 %)•Acta Orthopaedica: 3 articles (6 %)

Table 1 Top 7 journals and impact factors.

Journal	Publications	Impact Factor
Clinical Orthopaedics and Related Research (CORR)	14	4.4
Journal of the American Academy of Orthopaedic Surgeons (JAAOS)	5	3.2
Journal of Bone Oncology	3	3.5
Acta Orthopaedica	3	2.5
International Orthopaedics	2	2.6
Journal of Bone & Joint Surgery (JBJS)	2	6.5
Journal of Orthopaedic Research	2	2.3

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Fig. 4 The top journals the impact factors.

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Collectively, these journals published 50 % of the top-cited studies.

Other prominent publication journals included:•International Orthopaedics: 2 articles (4 %)•Journal of Bone & Joint Surgery (JBJS): 2 articles (4 %)•Journal of Orthopaedic Research: 2 articles (4 %)

3.7

3.7 Keyword Co-occurrence and network analysis

A keyword co-occurrence analysis was performed using the abstracts of the top 50 most cited articles on long bone metastatic disease. Repeated terms were extracted and mapped into a co-occurrence network, where each node represents a unique keyword, and edges indicate how often two keywords appear together in the same abstract (Fig. 5).

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Fig. 5 Keyword co-occurrence network of the 50 most cited articles on long bone metastatic disease. Nodes represent keywords; lines indicate co-occurrence. Colours reflect thematic clusters: surgical (Green), prognostic/oncologic (Blue), and outcomes/complications (Red).

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The most commonly recurring terms included:•“metastatic bone disease”•“pathological fracture”•“intramedullary nailing”•“endoprosthesis”•“surgery”•“Mirels score”•“prognosis”

Three thematic clusters were identified within the network analysis:1.Surgical Management Cluster (Green): The largest cluster, encompassing terms related to fixation techniques (intramedullary nailing, endoprosthetic reconstruction, plating), surgical outcomes, and implant survival.2.Prognostic and Oncologic Cluster (Blue): Included terms such as Mirels score, prognosis, survival, and risk stratification.3.Outcomes and Complications Cluster (Red): A smaller cluster centered on recurrence, revision, complications, and mortality

4 Discussion

Metastatic disease to the skeleton has a high incidence and long bones are involved in half of such skeletal metastatic cases.¹⁵ The increasing prevalence of this complex clinical condition highlights the need for evidence based management of these patients.⁷ To the best of our knowledge, this bibliometric analysis is the first on overall research trends on long bone metastasis. A previous analysis done in 2018 had it's primary focus on the surgical management of long bone metastasis which reflect the heavy focus on this aspect of research.¹⁶ Furthermore, 2 different bibliometric analysis in 2022 examined the available research on bone metastasis as a whole.^17,19 Our findings offer a unique overview of the available research on long bone metastasis disease as a whole.

This bibliometric analysis of the 50 most-cited articles on long bone metastatic disease reveals valuable insights into the evolving landscape of research within this critical area of orthopaedic oncology. The findings highlight a significant focus on surgical management, particularly strategies addressing treatment and prevention of pathological fractures resulting from metastatic lesions. The predominant citation of Mirels' foundational work underscores the enduring relevance of risk stratification tools in surgical decision-making.

A notable increase in publication activity during the 2000s reflects heightened awareness and clinical focus on managing skeletal metastases in recent years. This trend correlates with advancements in oncological therapies and improved survival rates for patients with metastatic cancer, contributing to more individuals potentially requiring surgical intervention due to skeletal manifestations of malignancy.^7,8

The absence of randomized controlled trials (RCTs) among the most-cited studies raises concerns about the robustness of the evidence base that informs current practices. A reliance on observational and retrospective cohort studies signifies a critical gap that must be addressed through well-designed prospective studies to yield high-level evidence. None of the 50 most-cited publications contain Level 1 or Level 2 evidence, which correlates with Kendal's bibliometric review in 2018.¹⁶

Geographical disparities in research outputs are evident, with a substantial concentration of high-impact articles from North America and Western Europe, capturing more than 70 % of the top publications. This concentration raises questions about the generalizability of findings across diverse populations and healthcare systems. A lack of significant contributions from low- and middle-income countries is particularly concerning, as these regions may face unique challenges regarding resources, patient demographics, and treatment modalities that differ from those in high-income countries. Expanding collaborative efforts globally could enhance the diversity and applicability of research in this area.

Keyword co-occurrence analysis identifies three significant thematic clusters: surgical management, prognostic and oncologic considerations, and outcomes and complications. The predominance of the surgical management cluster reflects the field's current emphasis on operative techniques as the primary approach to managing skeletal metastases. Scant attention is paid to complication analysis, patient experience and multidisciplinary management of these patients. Understanding the long-term impacts of surgical interventions on patients' quality of life and functional abilities is essential, especially given the growing importance of patient-centered care in modern medicine.

Limitations of this analysis are inherent to bibliometric methodologies. Reliance on Google Scholar via Publish or Perish software, while comprehensive, exposes the study to potential inclusion of non-peer-reviewed works and lacks the indexing rigor of traditional bibliometric databases. Citation counts do not directly reflect study quality or clinical significance. Older articles have more time to accumulate citation counts and do not necessarily reflect the current best practice evidence. Additionally, the analysis focused on the 50 most cited articles, potentially overlooking newer studies that have not reached high levels of exposure yet. Despite attempts to limit bias through discussions among authors, subjectivity in classifying levels of evidence may lead to disagreements. Notable findings of this analysis, which are themselves limitations of the long bone metastatic literature, were that the available research on bone metastasis consisted of low levels of evidence, poor representation of low and middle income countries and a disproportionate focus on surgical management.

Future research should prioritize expanding study populations to include underrepresented regions and diverse demographic groups. Elevating the quality of evidence through prospective RCTs and standardized outcome reporting will derive robust conclusions that can guide clinical decision-making. An increased focus on patient-centered outcomes, such as quality of life, pain management, and functional performance, will provide a more holistic view of treatment impacts. Furthermore, these patients present complex clinical problems that require a multidisciplinary approach including medical, surgical, nursing and allied health care. These features require better representation in the body of research in order to provide more wholistic care which is evidence based.

5 Conclusion

This bibliometric analysis offers a comprehensive overview of the most influential literature on long bone metastatic disease, revealing significant trends, strengths, and critical gaps within the current research landscape. A marked emphasis on surgical management strategies highlights the importance of preventing and addressing pathological fractures in patients with metastatic lesions. There is a need in the research for high levels of evidence research as well as better representation from low and middle income countries.

Opportunities exist to enhance the robustness of research on this topic as the population affected by long bone metastatic disease continues to grow. Expanding the scope of future research will improve understanding of long bone metastatic disease, ensuring that treatment strategies are effective and aligned with the holistic needs of patients facing this challenging condition.

Guardian/patient consent

Not Applicable.

Ethics

This study relied exclusively on publicly accessible bibliometric data and did not involve human participants or personal health information. As such, it was exempt from institutional review board approval and adhered to ethical standards governing secondary research.

Author contributions statement

•Nicolaas Kotze: Conceptualization, Data Curation, Formal Analysis, Manuscript Composition.

•Alexander Price: Data Curation, Formal Analysis, Manuscript Composition.

•Xander van Heerden: Formal Analysis, Manuscript Composition.

•Ruairí Mac Niocaill: Manuscript Review, Supervision.

•Paddy Kenny: Manuscript Review, Supervision.

•Joseph Queally: Manuscript Review, Supervision.

•Andrew Hughes: Manuscript Review, Supervision.

Funding

This research did not receive any specific grant from finding agencies in the public, commercial, or not-for-profit sectors.