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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Imaging response evaluation after neoadjuvant treatment in soft tissue sarcomas: Where do we stand?
Gennaro, N., Reijers, S. J. M., Bruining, A., Messiou, C., Haas, R. L., Colombo, P., Bodalal, Z., Beets‐Tan, R. G. H., van Houdt, W. J., & van der Graaf, W. T. A. (2021) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2021.103309 · Cited by 32
Dihydromyricetin suppresses cell metastasis in human osteosarcoma through SP-1- and NF-κB-modulated urokinase plasminogen activator inhibition
Chou, C., Lu, K., Yang, J., Hsieh, Y., Lin, C., & Yang, S. (2021) · Phytomedicine · doi:10.1016/j.phymed.2021.153642 · Cited by 30
Functional role of MicroRNA/PI3K/AKT axis in osteosarcoma
Xiang, Y., Yang, Y., Liu, J., & Yang, X. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1219211 · Cited by 30
A novel small molecule Met inhibitor, PF2362376, exhibits biological activity against osteosarcoma
Liao, A. T., McCleese, J., Kamerling, S. G., Christensen, J. G., & London, C. A. (2007) · Veterinary and Comparative Oncology · doi:10.1111/j.1476-5829.2007.00137.x · Cited by 30
Clinical Analysis of Osteosarcoma Patients Treated with High-Dose Methotrexate-Free Neoadjuvant Chemotherapy
Xu, M., Xu, S., & Yu, X. (2014) · Current Oncology · doi:10.3747/co.21.1973 · Cited by 30
Interferon‐γ sensitizes osteosarcoma cells to fas‐induced apoptosis by up‐regulating fas receptors and caspase‐8
Inaba, H., Glibetić, M., Buck, S. A., Ravindranath, Y., & Kaplan, J. (2004) · Pediatric Blood & Cancer · doi:10.1002/pbc.20151 · Cited by 30
“Treatment with neo-adjuvant chemotherapy, delivered in preoperative setting, has enabled us to evaluate histological responses and permitted less radical surgery by attacking the primary tumor and micro-metastasis [3].”
Background
Intraarterial Chemotherapy for Extremity Osteosarcoma and MFH in Adults
Hugate, R., Wilkins, R. M., Kelly, C. M., Madsen, W., Hinshaw, I., & Camozzi, A. B. (2008) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-008-0252-1 · Cited by 30
“Tumor necrosis is reportedly one of the most important prognostic factors impacting long-term survival in nonmetastatic osteosarcoma [ 9 , 15, 42].”
Background
Barriers to rehabilitation of patients with extremity sarcomas
Custodio, C. M. (2007) · Journal of Surgical Oncology · doi:10.1002/jso.20779 · Cited by 30
Comparisons of the Skeletal Locations of Putative Plutonium-Induced Osteosarcomas in Humans with those in Beagle Dogs and with Naturally Occurring Tumors in both Species
Miller, S. C., Lloyd, R. D., Bruenger, F. W., Krahenbuhl, M. P., Polig, E., & Romanov, S. A. (2003) · Radiation Research · doi:10.1667/rr3072 · Cited by 30
European standard clinical practice recommendations for children and adolescents with primary and recurrent osteosarcoma
van Ewijk, R., Herold, N., Baecklund, F., Baumhoer, D., Boye, K., Gaspar, N., Harrabi, S., Haveman, L., Hecker‐Nolting, S., Hiemcke‐Jiwa, L. S., et al. (2023) · EJC Paediatric Oncology · doi:10.1016/j.ejcped.2023.100029 · Cited by 33
Self-citation
p38 MAPK regulates the expression of ether à go-go potassium channel in human osteosarcoma cells
Wu, X., Zhong, D., Lin, B., Zhai, W., Ding, Z., & Wu, J. (2012) · Radiology and Oncology · doi:10.2478/v10019-012-0043-x · Cited by 29
Image navigation assisted joint-saving surgery for treatment of bone sarcoma around knee in skeletally immature patients
Li, J., Shi, L., & Chen, G. (2014) · Surgical Oncology · doi:10.1016/j.suronc.2014.04.004 · Cited by 29
Vascularized Fibula-Based Physis Transfer for Pediatric Proximal Humerus Reconstruction
Erdmann, D., Garcia, R. M., Blueschke, G., Brigman, B. E., & Levin, L. S. (2013) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e31829589fb · Cited by 29
Advances in Therapy for Pediatric Sarcomas
Weiss, A. R., Gill, J. B., Goldberg, J., Lagmay, J., Spraker‐Perlman, H. L., Venkatramani, R., & Reed, D. R. (2014) · Current Oncology Reports · doi:10.1007/s11912-014-0395-z · Cited by 28
“The ability to achieve complete surgical control of disease is required for cure, and the extent of tumor necrosis after neoadjuvant chemotherapy is another significant prognostic factor [7].”
Background
Comparison of the AJCC, MSTS, and Modified Spanier Systems for Clinical and Pathologic Staging of Osteosarcoma
Cates, J. (2017) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000774 · Cited by 29
Dexmedetomidine Inhibits Osteosarcoma Cell Proliferation and Migration, and Promotes Apoptosis by Regulating miR-520a-3p
Wang, X., Xu, Y.-G., Chen, X., & Xiao, J. (2017) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/096504017x14982578608217 · Cited by 29
“After MG63 cells were transfected or treated with (1) mimic control, (2) miR-520a-3p mimics, (3) inhibitor control, (4) miR-520a-3p inhibitor, (5) DEX + inhibitor control, and (6) DEX + miR-520a-3p inhibitor, cell proliferation, migration, and apoptosis of MG63 cells were respectively detected.”
Method
Retracted
Team Approach: Osteosarcoma of the Distal Part of the Femur in Adolescents
Stitzlein, R. N., Wojcik, J. B., Sebro, R., Balamuth, N., & WEBER, K. L. (2017) · JBJS Reviews · doi:10.2106/jbjs.rvw.17.00030 · Cited by 29
Connective tissue growth factor stimulates osteosarcoma cell migration and induces osteosarcoma metastasis by upregulating VCAM-1 expression
Hou, C., Yang, R., & Tsao, Y.-T. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.06.015 · Cited by 29
Prognostic factors to survival of patients with chondroblastic osteosarcoma
Sun, H.-H., Chen, X., Cui, J., Zhou, Z., & Guo, K. (2018) · Medicine · doi:10.1097/md.0000000000012636 · Cited by 29
Clinical outcome of osteosarcoma and its correlation with programmed death-ligand 1 and T cell activation markers
Yoshida, K., Okamoto, M., Sasaki, J., Kuroda, C., Ishida, H., Ueda, K., Okano, S., Ideta, H., Kamanaka, T., Sobajima, A., et al. (2019) · OncoTargets and Therapy · doi:10.2147/ott.s198421 · Cited by 29
Circ_0010220-mediated miR-503-5p/CDCA4 axis contributes to osteosarcoma progression tumorigenesis
Li, J., Zhang, F., Li, H., Peng, F., Wang, Z., Peng, H., He, J., Li, Y., He, L., & Wei, L. (2020) · Gene · doi:10.1016/j.gene.2020.145068 · Cited by 29
Mesenchymal stem cells plus bone repair materials as a therapeutic strategy for abnormal bone metabolism: Evidence of clinical efficacy and mechanisms of action implied
Zhang, S., Xie, D., & Zhang, Q. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105851 · Cited by 31
Long Noncoding RNA GAS5: A New Factor Involved in Bone Diseases
Zhou, Z., Chen, J., Huang, Y., Liu, D., Chen, S., & Qin, S. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.807419 · Cited by 29
T2-weighted MRI radiomics in high-grade intramedullary osteosarcoma: predictive accuracy in assessing histologic response to chemotherapy, overall survival, and disease-free survival
White, L. M., Atinga, A., Naraghi, A., Lajkosz, K., Wunder, J. S., Ferguson, P. C., Tsoi, K. M., Griffin, A. M., & Haider, M. A. (2022) · Skeletal Radiology · doi:10.1007/s00256-022-04098-2 · Cited by 30
Loss of ATRX promotes aggressive features of osteosarcoma with increased NF-κB signaling and integrin binding
DeWitt, S. B., Plumlee, S. H., Brighton, H. E., Sivaraj, D., Martz, E. J., Zand, M., Kumar, V., Sheth, M. U., Floyd, W., Spruance, J., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.151583 · Cited by 29
“For patients who develop metastatic disease, the prognosis is particularly bleak: almost 70% of patients do not survive beyond 5 years (3).”
Background
SIRT2 promotes the viability, invasion and metastasis of osteosarcoma cells by inhibiting the degradation of Snail
Tian, Y., Liu, R., Hou, X., Gao, Z., Liu, X., & Zhang, W. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05388-2 · Cited by 29
“Due to its strong metastasis, osteosarcoma is associated with a high mortality rate, with a 5-year survival rate of approximately 50–60% [5].”
BackgroundInfluential
Immunotherapy for Bone and Soft Tissue Sarcomas
Uehara, T., Fujiwara, T., Takeda, K., Kunisada, T., Ozaki, T., & Udono, H. (2015) · BioMed Research International · doi:10.1155/2015/820813 · Cited by 30
“Standard treatment modalities include surgical resection, chemotherapy, and often radiotherapy [6–8].”
Method
Analysis of prognostic factors in 333 C hinese patients with high‐grade osteosarcoma treated by multidisciplinary combined therapy
Min, D., Lin, F., Shen, Z., Zheng, S., Tan, L., Yu, W., & Yao, Y. (2012) · Asia-Pacific Journal of Clinical Oncology · doi:10.1111/j.1743-7563.2012.01560.x · Cited by 29
TNF-alpha, TNF-beta, IL-6, IL-10, PECAM-1 and the MPO Inflammatory Gene Polymorphisms in Osteosarcoma
Oliveira, I. D., Petrilli, A. S., Tavela, M., Zago, M. A., & de Toledo, S. R. C. (2007) · Journal of Pediatric Hematology/Oncology · doi:10.1097/mph.0b013e3180587e69 · Cited by 29
Osteosarcoma after allogeneic bone marrow transplantation. A report of four cases from the Cooperative Osteosarcoma Study Group (COSS)
Bielack, S., Rerin, J., Dickerhoff, R., Dilloo, D., Kremens, B., von Stackelberg, A., Vormoor, J. H., Jürgens, H., & for the Cooperative German–Austrian–Swiss Osteosarcoma Study Group COSS (2003) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1703864 · Cited by 28
Self-citation
Prognostic significance of 18F-FDG uptake in primary osteosarcoma after but not before chemotherapy: a possible association with autocrine motility factor/phosphoglucose isomerase expression
Sato, J., Yanagawa, T., Dobashi, Y., Yamaji, T., Takagishi, K., & Watanabe, H. (2008) · Clinical & Experimental Metastasis · doi:10.1007/s10585-008-9147-5 · Cited by 29
“Response to preoperative chemotherapy is the most important prognostic factor in OS since the degree of drug-induced tumor necrosis is highly correlated with event-free survival [3, 6 ]. There have been several reports showing a positive correlation of histologically viable tumor tissue and FDG uptake such as a decrea…”
BackgroundInfluential
Photodynamic action of methylene blue in osteosarcoma cells in vitro
Guan, J., Lai, X., Wang, X., Leung, A. W., Zhang, H., & Xu, C. (2013) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2013.09.003 · Cited by 29
Improved Survival in Osteosarcoma Patients with Atypical Low Vascularization
Kunz, P., Fellenberg, J., Moskovszky, L. E., Sápi, Z., Krenács, T., Machado, I., Poeschl, J., Lehner, B., Szendrői, M., Ruef, P., et al. (2014) · Annals of Surgical Oncology · doi:10.1245/s10434-014-4001-2 · Cited by 29
Curcumin inhibits hypoxia-induced proliferation and invasion of MG-63 osteosarcoma cells via downregulating Notch1
Wang, Z., Zhang, K., Zhu, Y., Wang, D., Shao, Y., & Zhang, J. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.6159 · Cited by 29
“However, the 5-year survival rate of patients with metastasis remains 30% (2).”
Suppression of Osteosarcoma Cell Invasion by Chemotherapy Is Mediated by Urokinase Plasminogen Activator Activity via Up-Regulation of EGR1
Matsunoshita, Y., Ijiri, K., Ishidou, Y., Nagano, S., Yamamoto, T., Nagao, H., Komiya, S., & Setoguchi, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016234 · Cited by 29
“The Survival rates for patients treated with intensive multidrug chemotherapy and aggressive local control have been reported at 60–80% [1–5].”
Background
Proximal fibula resection in the treatment of bone tumours
Dieckmann, R., Gebert, C., Streitbürger, A., Henrichs, M. P., Dirksen, U., Rödl, R. W., Gosheger, G., & Hardes, J. (2011) · International Orthopaedics · doi:10.1007/s00264-010-1193-3 · Cited by 29
“For local control of bone tumours a wide resection is necessary [ 9 ].”
Background
Targeted inhibition of osteosarcoma tumor growth by bone marrow‐derived mesenchymal stem cells expressing cytosine deaminase/5‐fluorocytosine in tumor‐bearing mice
NguyenThai, Q., Sharma, N., Luong, D. H., Sodhi, S. S., Kim, J., Kim, N., Oh, S., & Jeong, D. K. (2015) · The Journal of Gene Medicine · doi:10.1002/jgm.2826 · Cited by 28
Intercalary Resection of the Tibia for Primary Bone Tumors: Are Vascularized Fibula Autografts With or Without Allografts a Durable Reconstruction?
Campanacci, D. A., Scanferla, R., Marsico, M., Scolari, F., Scoccianti, G., Beltrami, G., Delcroix, L., Innocenti, M., & Capanna, R. (2024) · Clinical Orthopaedics and Related Research · doi:10.1097/corr.0000000000003007 · Cited by 28
“The tibia is the second most-frequent site of primary bone tumors, after the femur [4, 5].”
Background
Targeting metastasis in paediatric bone sarcomas
Bull, E. C., Singh, A., Harden, A. M., Soanes, K., Habash, H., Toracchio, L., Carrabotta, M., Schreck, C., Shah, K. M., Riestra, P. V., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02365-z · Cited by 31
“Overt metastatic disease detected at presentation confers a poor outcome with 20% long term survival [81].”
In silico functional analyses and discovery of survivalassociated microRNA signatures in pediatric osteosarcoma
Sánchez-Díaz, P. C., Hsiao, T.-H., Zou, Y., Sugalski, A., Heim-Hall, J. M., Chen, Y., Langevin, A., & Hung, J. Y. (2014) · Oncoscience · doi:10.18632/oncoscience.85 · Cited by 28
“To this date, incomplete surgery remains the most important negative prognostic indicator, followed by poor response to preoperative chemotherapy, primary metastases, and axial location [4-8].”
Background
Role of Protein Phosphatase 2A in Osteoblast Differentiation and Function
Okamura, H., Yoshida, K., Morimoto, H., Teramachi, J., Ochiai, K., Haneji, T., & Yamamoto, A. (2017) · Journal of Clinical Medicine · doi:10.3390/jcm6030023 · Cited by 28
“Osteosarcoma arises from mesenchymal bone-forming cells and mainly occurs in the long bones, such as the distal femur, the proximal tibia, and the humerus [88].”

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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