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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
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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“These strata were based on studies showing that a shorter relapse-free interval and older age are prognostic for shorter OS in patients with osteosarcoma.”
From Lenvatinib Plus Ifosfamide and Etoposide in Children and Young Adults With Relapsed Osteosarcoma (2024) · cites this paper as [33]
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“In addition, patients with unresectable primary or metastatic disease at diagnosis and those with disease relapse have extremely poor outcomes 2,126 .”
From Osteosarcoma (2022) · cites this paper as [2]
In the citing paper
“Otherwise, intralesional or marginal resections increase local recurrence rate, which is associated with reduced overall survival 2,134 .”
From Osteosarcoma (2022) · cites this paper as [2]
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“Neoadjuvant chemotherapy response and surgical margins achieved after oncological resections are well-established prognostic factors for survival and LR in patients with osteosarcoma [4, 6].”
BackgroundResultDurnalı, A., Alkış, N., Cangür, Ş., Yükrük, F. A., İnal, A., Tokluoğlu, S., ŞEKER, M. M., Bal, Ö., Akman, T., İnanç, M., et al. (2013) · Medical Oncology · doi:10.1007/s12032-013-0624-6 · Cited by 78
“These findings about discrepancies between extremity and trunk [8, 15] and head and neck osteosarcomas are compatible with the previous reports [23–25].”
BackgroundResultByun, B. H., Kong, C., Park, J., Seo, Y., Lim, I., Choi, C. W., Cho, W. H., Jeon, D., Koh, J., Lee, S., et al. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.117697 · Cited by 78
“Because patients with pelvic and vertebral osteosarcoma (21), age greater than 40 y (22), and skip lesions (AJCC stage III) or distant metastases at initial presentation (AJCC stage IV) have previously been reported to have poor outcomes (4), such patients were excluded from the current study.”
BackgroundPrognostic 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) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0969 · Cited by 78
“This group was selected to avoid an imbalance between the two groups (low versus high MVD) concerning known adverse prognostic factors in osteosarcoma (6).”
BackgroundMethodInfluentialSelf-citationWang, B., Su, Y., Yang, Q., Lv, D., Zhang, W., Tang, K., Wang, H., Zhang, R., & Liu, Y. (2015) · Molecules and Cells · doi:10.14348/molcells.2015.2327 · Cited by 76
“The 5-year survival rate is about 65% for patients with localized osteosarcoma, however, it sharply declined to about 20% for these cases with metastasis (Bielack et al., 2002; Eccles et al., 2007; Hughes, 2009).”
BackgroundRetractedResearch models and mesenchymal/epithelial plasticity of osteosarcoma
Yu, X., Yustein, J. T., & Xu, J. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00600-w · Cited by 77
“OS patients older than 60 years are associated with a higher risk of metastatic disease [8].”
BackgroundCurrent Status and Prospects of Clinical Treatment of Osteosarcoma
Jiang, Z.-Y., Liu, J., Wang, X., Ma, Y., & Fu, D. (2022) · Technology in Cancer Research & Treatment · doi:10.1177/15330338221124696 · Cited by 79
“6 However, since 80% of patients with osteosarcoma have distant metastasis at the time of initial diagnosis, the prognosis is extremely poor regardless of the treatment taken by 20% to 30% of patients.(7) Therefore, improving the treatment efficacy and survival rate of patients with osteosarcoma remains an urgent issu…”
BackgroundRuggieri, P., Bosco, G., Pala, E., Errani, C., & Mercuri, M. (2010) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-010-1476-4 · Cited by 77
Mu, X., Isaac, C. E., Greco, N., Huard, J., & Weiss, K. R. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00143 · Cited by 77
“INTRODUCTION Osteosarcoma (OS), the most common primary malignancy of bone, usually occurs in the long bones of youths in the first and second decades of life (Bielack et al., 2002; Carrle and Bielack, 2006; Hayden and Hoang, 2006).”
BackgroundLiu, W., Zhao, Z., Wang, Y., Li, W., Su, Q., Jia, Q., Zhang, J., Zhang, X., Shen, J., & Yin, J. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0363-x · Cited by 80
Liu, J., Chen, P., Chang, T., & Hou, C. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01756-y · Cited by 79
Anderson, P. M., Meyers, P. A., Kleinerman, E. S., Venkatakrishnan, K., Hughes, D. P. M., Herzog, C. E., Huh, W. W., Sutphin, R. M., Vyas, Y. M., Shen, V., et al. (2013) · Pediatric Blood & Cancer · doi:10.1002/pbc.24686 · Cited by 75
“Surgery remains the cornerstone of successful osteosarcoma therapy in both non-metastatic and metastatic patients [6,14].”
BackgroundAseptic Loosening Rates in Distal Femoral Endoprostheses: Does Stem Size Matter?
Bergin, P. F., Noveau, J., Jelinek, J. S., & Henshaw, R. M. (2011) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-011-2081-x · Cited by 76
Ma, W., Zhang, X., Chai, J., Chen, P., Ren, P., & Gong, M. (2014) · Tumor Biology · doi:10.1007/s13277-014-2565-x · Cited by 74
“The response to chemotherapy was determined by histological analysis of the resected specimens according to the previous criteria [22].”
Dong, Y., Liu, K., Fan, L., Liang, W., Xu, T., Jiang, W., Lu, H., Jiang, J., Wang, C. C., Li, G., et al. (2020) · Cancer Letters · doi:10.1016/j.canlet.2019.12.041 · Cited by 74
A Review of the Association between Osteosarcoma Metastasis and Protein Translation
Osborne, T. S., & Khanna, C. (2012) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2011.12.007 · Cited by 73
“Today, patients with localized disease at presentation have a 65–70% chance of 5-year relapse-free survival (Bielack et al., 2002; Hayden and Hoang, 2006; Kansara and Thomas, 2007; Meyers, 2009).”
BackgroundCurrent Status and Prospects of Targeted Therapy for Osteosarcoma
Hu, Z., Wen, S., Huo, Z., Wang, Q., Zhao, J., Wang, Z., Chen, Y., Zhang, L., Zhou, F., Guo, Z., et al. (2022) · Cells · doi:10.3390/cells11213507 · Cited by 78
Bacci, G., Longhi, A., Ferrari, S., Briccoli, A., Donati, D. M., PAOLIS, M. D., & Versari, M. (2004) · Tumori Journal · doi:10.1177/030089160409000507 · Cited by 73
Mensah‐Osman, E., Thomas, D. G., Tabb, M. M., Larios, J. M., Hughes, D. P. M., Giordano, T. J., Lizyness, M. L., Rae, J. M., Blumberg, B., Hollenberg, P. F., et al. (2007) · Cancer · doi:10.1002/cncr.22479 · Cited by 73
“O steogenic sarcoma is the most common primary malignant bone tumor, occurring in approximately 1 out of every 100,000 people per year.(1) Resistance to chemotherapy remains a major obstacle to the successful treatment of osteosarcoma.”
BackgroundImpact of close surgical margin on local recurrence and survival in osteosarcoma
Li, X., Moretti, V. M., Ashana, A. O., & Lackman, R. D. (2011) · International Orthopaedics · doi:10.1007/s00264-011-1230-x · Cited by 76
Reddy, K., Wafa, H., Gaston, C. L., Grimer, R. J., Abudu, A., Jeys, L. M., Carter, S. R., & Tillman, R. M. (2015) · The Bone & Joint Journal · doi:10.1302/0301-620x.97b1.33924 · Cited by 72
A causal role for circulating miR-34b in osteosarcoma
Tian, Q., Jia, J., Ling, S., Liu, Y., Yang, S., & Shao, Z. (2013) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2013.08.024 · Cited by 71
Current concepts on the surgical and medical management of osteosarcoma
Siegel, H. J., & Pressey, J. G. (2008) · Expert Review of Anticancer Therapy · doi:10.1586/14737140.8.8.1257 · Cited by 71
Why do patients with radiation-induced sarcomas have a poor sarcoma-related survival?
Bjerkehagen, B., Småstuen, M. C., Hall, K. S., Skjeldal, S., Smeland, S., & Fosså, S. D. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.559 · Cited by 71
“…(bone and soft tissue) þ trunk wall (soft tissue including axillary region and groin) vs (2) central site: head and neck (bone and soft tissue), intrathoracic and intraabdominal (soft tissue and viscera), and axial skeleton including scapulae, clavicles, ribs and pelvic bones (Bielack et al, 2002).”
BackgroundKim, H. J., Chalmers, P. N., & Morris, C. D. (2010) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e328334581f · Cited by 72
Bacci, G., Longhi, A., Cesari, M., Versari, M., & Bertoni, F. (2006) · Cancer · doi:10.1002/cncr.21937 · Cited by 71
Bhattacharya, S., Chalk, A. M., Ng, A. J. M., Martin, T. J., Zannettino, A. C. W., Purton, L. E., Lü, J., Baker, E. K., & Walkley, C. R. (2016) · Oncogene · doi:10.1038/onc.2016.68 · Cited by 72
Katonis, P., Datsis, G., Karantanas, A. H., Kampouroglou, A., Lianoudakis, S., Licoudis, S., Papoutsopoulou, E., & Alpantaki, K. (2013) · Clinical Medicine Insights Oncology · doi:10.4137/cmo.s10099 · Cited by 74
What Is New in the miRNA World Regarding Osteosarcoma and Chondrosarcoma?
Palmini, G., Marini, F., & Brandi, M. L. (2017) · Molecules · doi:10.3390/molecules22030417 · Cited by 70
“These are very rare tumours characterized by a poor 5-year survival rate from the time of diagnosis, despite recent advances treatment [54] Hence, the scientific world has started to consider the role of miRNAs in these sarcomas in an attempt to elucidate the tumour aetiology.”
BackgroundGuideline for Limb‐Salvage Treatment of Osteosarcoma
Xu, M., Wang, Z., Yu, X., Lin, J., & Hu, Y. (2020) · Orthopaedic Surgery · doi:10.1111/os.12702 · Cited by 70
Zhou, X., Yan, N., Cornel, E. J., Cai, H., Xue, S., Xi, H., Fan, Z., He, S., & Du, J. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120345 · Cited by 70
Pan, Z., Cheng, D., Wei, X., Li, S.-J., Guo, H., & Yang, Q. (2021) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2020.117596 · Cited by 69
Neoadjuvant Chemotherapy for Osteosarcoma of the Extremity
Bacci, G., Forni, C., Ferrari, S., Longhi, A., Bertoni, F., Mercuri, M., Donati, D. M., Capanna, R., Bernini, G., Briccoli, A., et al. (2003) · Journal of Pediatric Hematology/Oncology · doi:10.1097/00043426-200311000-00006 · Cited by 70
Overexpression of the HER-2 oncogene does not play a role in high-grade osteosarcomas
Anninga, J., van de Vijver, M. J., Cleton-Jansen, A., Kristel, P., Taminiau, A. H. M., Nooij, M. A., Egeler, R. M., & Hogendoorn, P. C. W. (2003) · European Journal of Cancer · doi:10.1016/j.ejca.2003.10.025 · Cited by 70
“Metastatic disease, large tumor volume, older age at presentation, axial site of the tumour, histological subtype of OS and histological response on preoperative treatment all have been associated with poor outcome (2-4).”
BackgroundRyan, C. W., MONTAG, A. G., Hosenpud, J., Samuels, B. L., Hayden, J. B., Hung, A., Mansoor, A., Peabody, T. D., Mundt, A. J., & Undevia, S. D. (2008) · Cancer · doi:10.1002/cncr.23478 · Cited by 70
Ogura, K., Fujiwara, T., Yasunaga, H., Matsui, H., Jeon, D., Cho, W. H., Hiraga, H., Ishii, T., Yonemoto, T., Kamoda, H., et al. (2015) · Cancer · doi:10.1002/cncr.29575 · Cited by 69
“Recent studies have demonstrated a more favorable outcome, especially for patients with nonmetastatic osteosarcoma.(5,6) Five-year survival rates of 60% to 80% have been reported for patients receiving intensive multidrug chemotherapy and surgery for aggressive local control.”
Background
Metadata
- 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
- Published
- 2002-02-01
- Volume
- 20
- Issue
- 3
- Pages
- 776-790
- ISSN
- 0732-183X (ISSN-L)
- 1527-7755
- 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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