Cited by 2,393Sarcoma Diagnosis and TreatmentBone Tumor Diagnosis and TreatmentsOvarian cancer diagnosis and treatment

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Prognostic Factors in High-Grade Osteosarcoma of the Extremities or Trunk: An Analysis of 1,702 Patients Treated on Neoadjuvant Cooperative Osteosarcoma Study Group Protocols

Bielack, Stefan S., Kempf-Bielack, Beate, Delling, Günter, Exner, G. Ulrich, Flege, Silke, Helmke, Knut, Kotz, Rainer, Salzer-Kuntschik, Mechthild, Werner, Matthias, Winkelmann, Winfried, Zoubek, Andreas, Jürgens, Heribert, Winkler, Kurt·2002·Journal of Clinical Oncology

DOI 10.1200/jco.2002.20.3.776

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Abstract

PURPOSE: To define prognostic factors for response and long-term outcome for a wide spectrum of osteosarcomas, extending well beyond those of the typical young patient with seemingly localized extremity disease. PATIENTS AND METHODS: A total of 1,702 consecutive newly diagnosed patients with high-grade osteosarcoma of the trunk or limbs registered into the neoadjuvant studies of the Cooperative Osteosarcoma Study Group before July 1998 were entered into an analysis of demographic, tumor-related, and treatment-related variables, response, and survival. The intended therapeutic strategy included preoperative and postoperative chemotherapy with multiple agents as well as surgery of all operable lesions. RESULTS: Axial tumor site, male sex, and a long history of symptoms were associated with poor response to chemotherapy in univariate and multivariate analysis. Actuarial 10-year overall and event-free survival rates were 59.8% and 48.9%. Among the variables assessable at diagnosis, patient age (actuarial 10-year survival ≥ 40, 41.6%; < 40, 60.2%; P = .012), tumor site (axial, 29.2%; limb, 61.7%; P < .0001), and primary metastases (yes, 26.7%; no, 64.4%; P < .0001), and for extremity osteosarcomas, also size (≥ one third, 52.5%; < one third, 66.7%; P < .0001) and location within the limb (proximal, 49.3%; other, 63.9%; P < .0001), had significant influence on outcome. Two additional important prognostic factors were treatment related: response to chemotherapy (poor, 47.2%; good, 73.4%; P < .0001) and the extent of surgery (incomplete, 14.6%; macroscopically complete, 64.8%; P < .0001). All factors except age maintained their significance in multivariate testing, with surgical remission and histologic response emerging as the key prognostic factors. CONCLUSION: Tumor site and size, primary metastases, response to chemotherapy, and surgical remission are of independent prognostic value in osteosarcoma.

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Background
Prognostic value of p53 alterations in human osteosarcoma: a meta analysis.
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Retracted
Bempegaldesleukin ( BEMPEG ; NKTR ‐214) efficacy as a single agent and in combination with checkpoint‐inhibitor therapy in mouse models of osteosarcoma
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Background
The safety of current pharmacotherapeutic strategies for osteosarcoma
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Background
Predictive value of the systemic immune-inflammation index for cancer-specific survival of osteosarcoma in children
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Background
Pharmacogenetics of chemotherapy treatment response and -toxicities in patients with osteosarcoma: a systematic review
Hurkmans, E. G. E., Brand, A. C. A. M., Verdonschot, J. A. J., Loo, D. M. W. M. T., & Coenen, M. J. H. (2022) · BMC Cancer · doi:10.1186/s12885-022-10434-5 · Cited by 24
“Metastasis at diagnosis is the best validated predictor for treat-ment response [4, 10, 11].”
Circular RNA circEMB promotes osteosarcoma progression and metastasis by sponging miR-3184-5p and regulating EGFR expression
Tan, J., Yang, B., Zhong, H., Luo, M., Su, Z., Xie, C. L., Shi, M., Sun, C., & Lin, L. (2023) · Biomarker Research · doi:10.1186/s40364-022-00442-9 · Cited by 22
Cortactin (CTTN) overexpression in osteosarcoma correlates with advanced stage and reduced survival
Folio, C., Zalacaín, M., Zandueta, C., Ormazabal, C., Sierrasesúmaga, L., San-Julián, M., Rivas, J. D. L., Toledo, G., Lecanda, F., & Patiño‐García, A. (2012) · Cancer Biomarkers · doi:10.3233/cbm-2012-0227 · Cited by 22
Regenerative therapy with mesenchymal stem cells at the site of malignant primary bone tumour resection: what are the risks of early or late local recurrence?
Hernigou, P., Flouzat Lachaniette, C. H., Delambre, J., Chevallier, N., & Rouard, H. (2014) · International Orthopaedics · doi:10.1007/s00264-014-2384-0 · Cited by 22
“6 % that appears to conform to the other series in the literature [2, 3, 14, 15, 17, 28, 29, 39] for the main tumours (osteosarcoma, chondrosarcoma, and Ewing sarcoma).”
Effect of neoadjuvant treatment in the management of osteosarcomas of the head and neck
Mücke, T., Mitchell, D. A., Tannapfel, A., Wolff, K., Loeffelbein, D. J., & Kanatas, A. N. (2013) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-013-1550-x · Cited by 25
“The histological analysis of excised tumors is the most reliable method to assess the response to chemotherapy, and the significance of this method in the prognosis of patients with osteosarcoma is well documented (Bielack et al. 2002; Davis et al. 1994; Miwa et al. 2013) At present, it is not possible to assess chemo…”
Method
Efficacy of a nitrogen-containing bisphosphonate, minodronate, in conjunction with a p38 mitogen activated protein kinase inhibitor or doxorubicin against malignant bone tumor cells
Kubo, T., Shimose, S., Matsuo, T., Sakai, A., & Ochi, M. (2007) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-007-0580-y · Cited by 22
“Despite significant improvement in patient survival rates by intensifying chemotherapy protocols, some groups of patients with unresectable primary tumors, like intense pelvic lesion, and those with clinically evident metastases still have a poor prognosis even in chemotherapy-responsive osteosarcoma and Ewing’s sarco…”
Background
Upper Extremity Considerations for Oncologic Surgery
Wong, J. C., & Abraham, J. A. (2014) · Orthopedic Clinics of North America · doi:10.1016/j.ocl.2014.06.007 · Cited by 22
“Prognostic factors for survival include tumor size and location, presence of systemic or skip metastases at the time of presentation, and response to neoadjuvant chemotherapy.(26,27) Increase of serum markers such as lactate dehydrogenase and alkaline phosphatase are also associated with risk of relapse.”
Background
Osteosarcomas in the upper distal extremities: Are their oncological outcomes similar to other sites?
Pradhan, A., Reddy, K., Grimer, R. J., Abudu, A., Tillman, R. M., Carter, S. R., & Jeys, L. M. (2014) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2014.11.038 · Cited by 22
Mechanisms of therapy resistance in osteosarcoma: a review
PosthumaDeBoer, J., van Royen, B. J., & Helder, M. N. (2013) · Oncology Discovery · doi:10.7243/2052-6199-1-8 · Cited by 22
“However, in the case of metastatic or recurrent disease, 5-year survival rates are reduced to only 20% [1-5].”
Background
Polymeric immunoglobulin receptor expression is correlated with poor prognosis in patients with osteosarcoma
Wang, X., Du, J., Gu, P., Jin, R., & Lin, X. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2110 · Cited by 21
“Despite aggressive treatment modalities, including high-dose chemotherapy and wide tumor resection, the five‐year survival rate for patients with osteosarcoma is between 55 and 60% and <40% for patients with pulmonary metastases (4,5).”
Does Competing Risk Analysis Give Useful Information About Endoprosthetic Survival in Extremity Osteosarcoma?
Schuh, R., Kaider, A., Windhager, R. H., & Funovics, P. T. (2014) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-014-3703-x · Cited by 22
“Consequently, reconstructive failures remain relatively common and are caused by local tumor recurrence, infection, aseptic loosening, and fracture, among others [1, 4, 5, 12, 14, 16, 19, 20].”
Background
Post‐genomics of bone metabolic dysfunctions and neoplasias
Bernardini, G., Braconi, D., Spreafico, A., & Santucci, A. (2012) · PROTEOMICS · doi:10.1002/pmic.201100358 · Cited by 22
Prognostic relevance of the mitotic count and the amount of viable tumour after neoadjuvant chemotherapy for primary, localised, high-grade soft tissue sarcoma
Andreou, D., Werner, M., Pink, D., Traub, F., Schuler, M. K., Gosheger, G., Jobke, B., Reichardt, P., & Tunn, P. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.635 · Cited by 22
“DISCUSSION The histological assessment of tumour response to neoadjuvant chemotherapy is one of the most important prognostic factors in osteosarcoma (Bielack et al, 2002) and Ewing sarcoma (Picci et al, 1993).”
BackgroundSelf-citation
Osteosarcoma in Patients with Rothmund–Thomson Syndrome
Zils, K., Klingebiel, T. E., Behnisch, W., Muller, H. L., Schlegel, P., Fruehwald, M., Suttorp, M., Simon, T., Werner, M., & Bielack, S. (2014) · Pediatric Hematology and Oncology · doi:10.3109/08880018.2014.987939 · Cited by 22
“The age of our patients was somewhat younger to that of sporadic osteosarcoma, which is 15 years [21, 22] but older than reported for osteosarcoma in other published RTS patients (10 years) [20].”
BackgroundResultSelf-citation
High Expression of XRCC6 Promotes Human Osteosarcoma Cell Proliferation through the β-Catenin/Wnt Signaling Pathway and Is Associated with Poor Prognosis
Zhu, B., Cheng, D., Li, S.-J., Zhou, S., & Yang, Q. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071188 · Cited by 22
“However, treating metastatic and recurrent OS with current treatments is still limited [6].”
MicroRNA-187 Inhibits Growth and Metastasis of Osteosarcoma by Downregulating S100A4
Xiao, Y., Zhao, Q., Du, B. X., Chen, H.-Y., & Dao-zheng, Z. (2018) · Cancer Investigation · doi:10.1080/07357907.2017.1415348 · Cited by 22
“Although the efficiency of the major therapies, including chemotherapy, radiotherapy, and tumor excision strategies has improved significantly, the clinical outcome of OS patients remains unsatisfactory, especially for those at an advanced stage (3).”
Background
Immunoconjugates for Osteosarcoma Therapy: Preclinical Experiences and Future Perspectives
Mercatelli, D., Bortolotti, M., Bazzocchi, A., Bolognesi, A., & Polito, L. (2018) · Biomedicines · doi:10.3390/biomedicines6010019 · Cited by 22
“Typically occurring during the adolescent growth spurt, with a peak in the second decade of life and a higher incidence in males, OS shows a bimodal distribution with a second peak in the population over 65 years old, frequently associated with prior radiation therapy or Paget’s disease [5].”
Background
The prognosis for patients with osteosarcoma who have received prior manipulative therapy
Wu, P., Chen, W.-M., Lee, O. K., Chen, C., Huang, C., & Chen, T.-H. (2010) · Journal of Bone and Joint Surgery - British Volume · doi:10.1302/0301-620x.92b11.24706 · Cited by 22
Comparison of the Outcome of Conventional Osteosarcoma at Two Specialist International Orthopaedic Oncology Centres
Ford, S., Saithna, A., Grimer, R. J., & Picci, P. (2004) · Sarcoma · doi:10.1080/13577140410001679202 · Cited by 22
Tumours of the Hand: a Review On Histology of Bone Malignancies
Baumhoer, D., & Jundt, G. (2010) · Journal of Hand Surgery (European Volume) · doi:10.1177/1753193409358382 · Cited by 22
“The rationale behind this concept is that osteosarcoma is regarded a systemic disease at the time of diagnosis and almost invariably has already seeded microscopic lung metastases (Bielack et al., 2002).”
Prognostic relevance of increased angiogenesis in osteosarcoma
Kreuter, M., Bieker, R., Bielack, S., Auras, T., Buerger, H., Gosheger, G., Jürgens, H., Berdel, W. E., & Mesters, R. M. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.22.90140.9022 · Cited by 22
Self-citation
Biomaterials‐Boosted Immunotherapy for Osteosarcoma
Sun, C., Li, S., & Ding, J. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202400864 · Cited by 25
Modulating tumor-associated macrophage polarization by anti-maRCO mAb exerts anti-osteosarcoma effects through regulating osteosarcoma cell proliferation, migration and apoptosis
Ding, L., Wu, L., Cao, Y., Wang, H., Li, D., Chen, W., Huang, P., & Jiang, Z. (2024) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-024-04950-2 · Cited by 21
“Consequently, new research on treat-ment methods has become a prominent subject in basic and clinical research [8].”
Background
Efficacy and safety of apatinib in advance osteosarcoma with pulmonary metastases
Zheng, K., Xu, M., Wang, L., & Yu, X. (2018) · Medicine · doi:10.1097/md.0000000000011734 · Cited by 21
Dihydrotanshinone I inhibits the growth of osteosarcoma through the Wnt/β-catenin signaling pathway
Tan, T., Chen, J., Hu, Y., Wang, N., Chen, Y., Yu, T., Lin, D., Yang, S., Luo, J., & Luo, X. (2019) · OncoTargets and Therapy · doi:10.2147/ott.s204574 · Cited by 21
Retracted
The effect of preoperative radiotherapy on local control and prognosis in high-grade non-metastatic intramedullary osteosarcoma of the extremities
Hız, M., Karaismailoğlu, B., Ulutaş, S., Camurdan, V. B., Görgün, B., & Dinçbaş, F. Ö. (2020) · Archives of Orthopaedic and Trauma Surgery · doi:10.1007/s00402-020-03494-4 · Cited by 21
“also claimed that the histologic response is one of the key prognostic factors [11].”
Background
Bromodomain Inhibition Attenuates the Progression and Sensitizes the Chemosensitivity of Osteosarcoma by Repressing GP130/STAT3 Signaling
Jiang, Y., Wang, G., Mu, H., Ma, X., Wang, Z., Lv, Y. B., Zhang, T., Xu, J., Wang, J., Li, Y., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.642134 · Cited by 21
“Osteosarcoma usually occurs in the metaphysis of long bones, most commonly in the distal femur (43%), proximal tibia (23%), and humerus (10%) (1).”
Background
Impact of racial disparities and insurance status in patients with bone sarcomas in the USA
Hu, X., Fujiwara, T., Houdek, M. T., Chen, L., Huang, W., Sun, Z., Sun, Y., & Yan, W. (2022) · Bone and Joint Research · doi:10.1302/2046-3758.115.bjr-2021-0258.r2 · Cited by 21
Insight into the interplay between mitochondria-regulated cell death and energetic metabolism in osteosarcoma
Lai, H.-T., Naumova, N., Marchais, A., Gaspar, N., Geoerger, B., & Brenner, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.948097 · Cited by 23
“The disease demonstrates a high degree of malignancy and has a tendency to metastasize at early stages (Bielack et al., 2002).”
Background
Der proximale und komplette Femurersatz
Pennekamp, P. H., Wirtz, D. C., & Dürr, H. R. (2012) · Operative Orthopädie und Traumatologie · doi:10.1007/s00064-011-0061-7 · Cited by 21
Stratifying Osteosarcoma: Minimizing and Maximizing Therapy
Niswander, L. M., & Kim, S. Y. (2010) · Current Oncology Reports · doi:10.1007/s11912-010-0106-3 · Cited by 21
“The vast majority of osteosarcoma originates in the metaphysis of long bones, and before the 1980 s treatment involved amputation of the affected extremity when possible [ 3 ].”
BackgroundInfluential
Tumor necrosis in osteosarcoma: inclusion of the point of greatest metabolic activity from F-18 FDG PET/CT in the histopathologic analysis
Costelloe, C. M., Raymond, A. K., Fitzgerald, N. E., Mawlawi, O. R., NUÑEZ, R. F., Madewell, J. E., Harrell, R. K., Bassett, R. L., & Marom, E. M. (2009) · Skeletal Radiology · doi:10.1007/s00256-009-0785-8 · Cited by 21
Comparative proteomic analysis of human osteosarcoma and SV40-immortalized normal osteoblastic cell lines
Guo, Q., Jing-nan, S. H. E. N., Jin, S., Wang, J., HUANG, G., Zhang, L., Yin, J., Zou, C., & Ming-tao, L. I. (2007) · Acta Pharmacologica Sinica · doi:10.1111/j.1745-7254.2007.00603.x · Cited by 21
Osteosarcoma presentation stages at a tumour unit in South Africa
Ferreira, N., & Marais, L. C. (2012) · South African Medical Journal · doi:10.7196/samj.5835 · Cited by 22
Cisplatin-resistant osteosarcoma cells possess cancer stem cell properties in a mouse model
Yang, J., Guo, W., Wang, L., Yu, L., Mei, H., Fang, S., Ji, P., Liu, Y., Liu, G., & Song, Q. (2016) · Oncology Letters · doi:10.3892/ol.2016.4956 · Cited by 21
“Osteosarcoma is the most frequent primary malignancy of bone tissue, which mostly occurs in adolescents and children, comprising almost 60% of all bone sarcomas (1,2).”
Suberanilohydroxamic acid (vorinostat) synergistically enhances the cytotoxicity of doxorubicin and cisplatin in osteosarcoma cell lines
Pettke, A., Hotfilder, M., Clemens, D., Klco‐Brosius, S., Schaefer, C., Potratz, J. C., & Dirksen, U. (2016) · Anti-Cancer Drugs · doi:10.1097/cad.0000000000000418 · Cited by 21
FDG PET/CT appearance of local osteosarcoma recurrences in pediatric patients
Sharp, S. E., Shulkin, B. L., Gelfand, M. J., & McCarville, M. B. (2017) · Pediatric Radiology · doi:10.1007/s00247-017-3963-1 · Cited by 21
Inhibition of NADPH oxidase 2 induces apoptosis in osteosarcoma: The role of reactive oxygen species in cell proliferation
Kitamoto, K., Miura, Y., Karnan, S., Ota, A., Konishi, H., Hosokawa, Y., & Sato, K. (2018) · Oncology Letters · doi:10.3892/ol.2018.8291 · Cited by 21
MiR-1 Suppresses Proliferation of Osteosarcoma Cells by Up-regulating p21 via PAX3
FUJII, R., Osaka, E., Sato, K., & Tokuhashi, Y. (2018) · Cancer Genomics & Proteomics · doi:10.21873/cgp.20113 · Cited by 21
Nitidine Chloride Inhibits SIN1 Expression in Osteosarcoma Cells
Xu, H., Cao, T., Zhang, X., Shi, Y., Zhang, Q., Chai, S., Li, Y., Jin, G., Ma, J., Wang, Z. P., et al. (2019) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2019.01.005 · Cited by 21
“Although treatment of osteosarcoma has been improved, metastatic osteosarcoma patients often have poor prognoses and they relapse.(4) Discovery of new therapeutic agents is pivotal to improving the treatment outcome in osteosarcoma patients.”
Background

Authors: Bielack, S. S., Kempf-Bielack, B., Delling, G., Exner, G. U., Flege, S., Helmke, K., Kotz, R., Salzer-Kuntschik, M., Werner, M., Winkelmann, W., Zoubek, A., Jürgens, H., & Winkler, K.
Affiliations: University of Münster (DE)
Corresponding author: Bielack, Stefan S.
ORCID: Bielack, Stefan S.
Venue: Journal of Clinical Oncology
Publisher: American Society of Clinical Oncology (ASCO)
Published: 2002-02-01
Volume: 20
Issue: 3
Pages: 776-790
ISSN: 0732-183X (ISSN-L)
1527-7755
DOI: 10.1200/jco.2002.20.3.776
OpenAlex: W2148077417
Cited by: 2,393
References: 61
Citations by year: 2026: 85 · 2025: 95 · 2024: 112 · 2023: 162 · 2022: 159 · 2021: 167 · 2020: 166 · 2019: 121 · 2018: 114 · 2017: 106 · 2016: 122 · 2015: 139 · 2014: 124 · 2013: 106 · 2012: 75
FWCI: 34.99
Type: journal article
Language: en
Update notices: new_edition (2023-09-15)
Open access: closed
Locations: Journal of Clinical Oncology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Oncology › Sarcoma Diagnosis and Treatment
Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone Tumor Diagnosis and Treatments
Health Sciences › Medicine › Oncology › Ovarian cancer diagnosis and treatment
Keywords: high-grade osteosarcoma, prognostic factors, neoadjuvant chemotherapy, limb-sparing surgery, tumor location, tumor size, chemotherapy response, surgical remission, event-free survival, overall survival, histological response, patient age, sex differences
MeSH terms: Adolescent, Adult, Aged, Bone Neoplasms, Child, Child, Preschool, Combined Modality Therapy, Female, Humans, Male, Middle Aged, Neoplasm Metastasis, Prognosis, Osteosarcoma, Survival Rate, Multivariate Analysis, Chemotherapy, Adjuvant

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Prognostic Factors in High-Grade Osteosarcoma of the Extremities or Trunk: An Analysis of 1,702 Patients Treated on Neoadjuvant Cooperative Osteosarcoma Study Group Protocols

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