Bone metastases in lung cancer

Main Article Content

Maria Beatrice Bocchi Luigi Cianni Tommaso Greco Giulio Maccauro Carlo Perisano

Abstract

As lung cancer is the most common neoplasm worldwide, bone is one of the most metastatic sites of advanced malignant tumors in general. Nearly 50% of patients with advanced lung cancer develop bone metastases. A literature review on this matter was performed.


As in recent years the life expectancy of patients with lung cancer increased, symptoms control measures are gaining importance. The early detection of bone metastases is crucial due to prevent skeletal-related events (SREs). The bone metastases management should be discussed in a multidisciplinary setting given the numerous therapeutic options. Treatment is either pharmacological (analgesics, diphosphonates, monoclonal antibodies), non-pharmacological (radiotherapy, interventional radiological techniques, surgery) or even a combination of both. Orthopedic surgery shall be assessed in case of pathological/impending fractures. The orthopedic surgeon challenge is indeed to detect those patients who will take advantage from surgery given the substantial risk of complications. Treatment goal should be to obtain SREs prevention and control to guarantee patients a decent QoL. Unfortunately, bone metastases in lung cancer are still poor prognosis indicator.

Keywords: lung cancer, NSCLC, bone metastases, BM, skeletal-related events, SREs, pathological fracture, impending fracture, pain, pain control, hypercalcemia, spinal cord compression, SCC, Denosumab, Bisphosphonates, Zoledronate, radiotherapy, RT, prosthetic reconstruction, megaprosthesis, intramedullary nailing, PMMA, cementoplasty, vertebroplasty, kyphoplasty

Article Details

How to Cite
BOCCHI, Maria Beatrice et al. Bone metastases in lung cancer. Medical Research Archives, [S.l.], v. 9, n. 2, feb. 2021. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/2339>. Date accessed: 18 apr. 2024. doi: https://doi.org/10.18103/mra.v9i2.2339.
Section
Research Articles

References

1. IARC. Cancer Incidence, Mortality and Prevalence Worldwide GLOBOCAN, 2020. See: https://gco.iarc.fr/.
2. EC. ECIS, 2020. See: https://ecis.jrc.ec.europa.eu/.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90. doi:10.3322/caac.20107
4. Ordóñez-Mena JM, Schöttker B, Mons U, et al. Quantification of the smoking-associated cancer risk with rate advancement periods: meta-analysis of individual participant data from cohorts of the CHANCES consortium. BMC Med. 2016;14:62. doi:10.1186/s12916-016-0607-5
5. Malhotra J, Malvezzi M, Negri E, La Vecchia C, Boffetta P. Risk factors for lung cancer worldwide. Eur Respir J. 2016;48(3):889-902. doi:10.1183/13993003.00359-2016
6. Hashim D, Boffetta P, La Vecchia C, et al. The global decrease in cancer mortality: trends and disparities. Ann Oncol. 2016;27(5):926-933. doi:10.1093/annonc/mdw027
7. IARC. Cancer Incidence, Mortality and Prevalence Worldwide GLOBOCAN 2012. See: http://gco.iarc.fr.
8. Toh C-K, Gao F, Lim W-T, et al. Never-smokers with lung cancer: epidemiologic evidence of a distinct disease entity. J Clin Oncol. 2006;24(15):2245-2251. doi:10.1200/JCO.2005.04.8033
9. Couraud S, Souquet P-J, Paris C, et al. BioCAST/IFCT-1002: epidemiological and molecular features of lung cancer in never-smokers. Eur Respir J. 2015;45(5):1403-1414. doi:10.1183/09031936.00097214
10. Villalobos P, Wistuba II. Lung Cancer Biomarkers. Hematol Oncol Clin North Am. 2017;31(1):13-29. doi:10.1016/j.hoc.2016.08.006
11. D’Addario G, Früh M, Reck M, et al. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2010;21 Suppl 5:v116-119. doi:10.1093/annonc/mdq189
12. Cagle PT, Allen TC, Olsen RJ. Lung cancer biomarkers: present status and future developments. Arch Pathol Lab Med. 2013;137(9):1191-1198. doi:10.5858/arpa.2013-0319-CR
13. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med. 2006;355(24):2542-2550. doi:10.1056/NEJMoa061884
14. Doroshow DB, Sanmamed MF, Hastings K, et al. Immunotherapy in Non-Small Cell Lung Cancer: Facts and Hopes. Clin Cancer Res. 2019;25(15):4592-4602. doi:10.1158/1078-0432.CCR-18-1538
15. Zhou C, Wu Y-L, Chen G, et al. EFFICACY RESULTS FROM THE RANDOMISED PHASE III OPTIMAL (CTONG 0802) STUDY COMPARING FIRST-LINE ERLOTINIB VERSUS CARBOPLATIN (CBDCA) PLUS GEMCITABINE (GEM), IN CHINESE ADVANCED NON-SMALL-CELL LUNG CANCER (NSCLC) PATIENTS (PTS) WITH EGFR ACTIVATING MUTATIONS.; 2010:6.
16. Yang Z, Hackshaw A, Feng Q, et al. Comparison of gefitinib, erlotinib and afatinib in non-small cell lung cancer: A meta-analysis. Int J Cancer. 2017;140(12):2805-2819. doi:10.1002/ijc.30691
17. Lima ABC, Macedo LT, Sasse AD. Addition of bevacizumab to chemotherapy in advanced non-small cell lung cancer: a systematic review and meta-analysis. PLoS One. 2011;6(8):e22681. doi:10.1371/journal.pone.0022681
18. Leighl NB, Karaseva N, Nakagawa K, et al. Patient-reported outcomes from FLAURA: Osimertinib versus erlotinib or gefitinib in patients with EGFR-mutated advanced non-small-cell lung cancer. Eur J Cancer. 2020;125:49-57. doi:10.1016/j.ejca.2019.11.006
19. Gandara DR, Paul SM, Kowanetz M, et al. Blood-based tumor mutational burden as a predictor of clinical benefit in non-small-cell lung cancer patients treated with atezolizumab. Nat Med. 2018;24(9):1441-1448. doi:10.1038/s41591-018-0134-3
20. Velcheti V, Kim ES, Mekhail T, et al. Prospective clinical evaluation of blood-based tumor mutational burden (bTMB) as a predictive biomarker for atezolizumab (atezo) in 1L non-small cell lung cancer (NSCLC): Interim B-F1RST results. JCO. 2018;36(15_suppl):12001-12001. doi:10.1200/JCO.2018.36.15_suppl.12001
21. Kuchuk M, Kuchuk I, Sabri E, Hutton B, Clemons M, Wheatley-Price P. The incidence and clinical impact of bone metastases in non-small cell lung cancer. Lung Cancer. 2015;89(2):197-202. doi:10.1016/j.lungcan.2015.04.007
22. Wang H, Zhang Y, Zhu H, Yu J. Risk factors for bone metastasis in completely resected non-small-cell lung cancer. Future Oncol. 2017;13(8):695-704. doi:10.2217/fon-2016-0237
23. Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res. 2006;12(20 Pt 2):6243s-6249s. doi:10.1158/1078-0432.CCR-06-0931
24. Coello MC, Luketich JD, Litle VR, Godfrey TE. Prognostic significance of micrometastasis in non-small-cell lung cancer. Clin Lung Cancer. 2004;5(4):214-225. doi:10.3816/CLC.2004.n.002
25. Tokuhashi Y, Matsuzaki H, Toriyama S, Kawano H, Ohsaka S. Scoring system for the preoperative evaluation of metastatic spine tumor prognosis. Spine (Phila Pa 1976). 1990;15(11):1110-1113. doi:10.1097/00007632-199011010-00005
26. Akhtar M, Haider A, Rashid S, Al-Nabet ADMH. Paget’s “Seed and Soil” Theory of Cancer Metastasis: An Idea Whose Time has Come. Adv Anat Pathol. 2019;26(1):69-74. doi:10.1097/PAP.0000000000000219
27. Fornetti J, Welm AL, Stewart SA. Understanding the Bone in Cancer Metastasis. J Bone Miner Res. 2018;33(12):2099-2113. doi:10.1002/jbmr.3618
28. Kan C, Vargas G, Pape FL, Clézardin P. Cancer Cell Colonisation in the Bone Microenvironment. Int J Mol Sci. 2016;17(10). doi:10.3390/ijms17101674
29. Stomeo D, Tulli A, Ziranu A, Perisano C, De Santis V, Maccauro G. Acrometastasis: a literature review. Eur Rev Med Pharmacol Sci. 2015;19(15):2906-2915.
30. Greco T, Cianni L, De Mauro D, et al. Foot metastasis: Current knowledge. Orthop Rev (Pavia). 2020;12(Suppl 1):8671. doi:10.4081/or.2020.8671
31. Perisano C, Vitiello R, Greco T, et al. A report of a very rare isolated bone metastasis in the midfoot due to cervix cancer. Minerva Ortop Traumatol. 2019;70(2). doi:10.23736/S0394-3410.19.03918-3
32. Morikawa K, Mineshita M, Nishine H, Furuya N, Obayashi J, Miyazawa T. A Case of Squamous Cell Lung Carcinoma with Bone Metastasis Responding to Denosumab After Zoledronic Acid Hydrate. Haigan. 2012;52(7):1035-1040. doi:10.2482/haigan.52.1035
33. Perisano C, Scaramuzzo L, De Santis V, et al. QUALITY OF LIFE FOLLOWING SURGICAL TREATMENT OF LOWER LIMB METASTASES IN LONG BONE. J Biol Regul Homeost Agents. 2015;29(2):501-507.
34. Delea T, Langer C, McKiernan J, et al. The cost of treatment of skeletal-related events in patients with bone metastases from lung cancer. Oncology. 2004;67(5-6):390-396. doi:10.1159/000082923
35. Schulman KL, Kohles J. Economic burden of metastatic bone disease in the U.S. Cancer. 2007;109(11):2334-2342. doi:10.1002/cncr.22678
36. Santini D, Daniele S, Barni S, et al. Natural History of Non-Small-Cell Lung Cancer with Bone Metastases. Sci Rep. 2015;5:18670. doi:10.1038/srep18670
37. Berruti A, Dogliotti L, Gorzegno G, et al. Differential patterns of bone turnover in relation to bone pain and disease extent in bone in cancer patients with skeletal metastases. Clin Chem. 1999;45(8 Pt 1):1240-1247.
38. Oliveira MBDR, Marques B de C, Matos RA, Fontenelle CR da C, Mello FC de Q, Paschoal MEM. PATHOLOGICAL FRACTURES DUE TO BONE METASTASES FROM LUNG CANCER: RISK FACTORS AND SURVIVAL. Acta Ortop Bras. 2018;26(6):388-393. doi:10.1590/1413-785220182606201669
39. Enneking W, Dunham W, Gebhardt M, Malawar M, Pritchard D. A system for the classification of skeletal resections. Chir Organi Mov. 1990;75(1 Suppl):217-240.
40. Müller DA, Capanna R. The surgical treatment of pelvic bone metastases. Adv Orthop. 2015;2015:525363. doi:10.1155/2015/525363
41. Cetin K, Christiansen CF, Jacobsen JB, Nørgaard M, Sørensen HT. Bone metastasis, skeletal-related events, and mortality in lung cancer patients: a Danish population-based cohort study. Lung Cancer. 2014;86(2):247-254. doi:10.1016/j.lungcan.2014.08.022
42. Maccauro G, Spinelli MS, Mauro S, Perisano C, Graci C, Rosa MA. Physiopathology of spine metastasis. Int J Surg Oncol. 2011;2011:107969. doi:10.1155/2011/107969
43. Sutcliffe P, Hummel S, Simpson E, et al. Use of classical and novel biomarkers as prognostic risk factors for localised prostate cancer: a systematic review. Health Technol Assess. 2009;13(5):iii, xi-xiii 1-219. doi:10.3310/hta13050
44. Janjan NA. Radiation for bone metastases: conventional techniques and the role of systemic radiopharmaceuticals. Cancer. 1997;80(8 Suppl):1628-1645. doi:10.1002/(sici)1097-0142(19971015)80:8+<1628::aid-cncr13>3.3.co;2-l
45. Sutcliffe P, Connock M, Shyangdan D, Court R, Kandala N-B, Clarke A. A systematic review of evidence on malignant spinal metastases: natural history and technologies for identifying patients at high risk of vertebral fracture and spinal cord compression. Health Technol Assess. 2013;17(42):1-274. doi:10.3310/hta17420
46. Riley RD, Burchill SA, Abrams KR, et al. A systematic review of molecular and biological markers in tumours of the Ewing’s sarcoma family. Eur J Cancer. 2003;39(1):19-30. doi:10.1016/s0959-8049(02)00500-2
47. Lee JH, Stein M, Roychowdhury S. Percutaneous treatment of a sacral metastasis with combined embolization, cryoablation, alcohol ablation and sacroplasty for local tumor and pain control. Interv Neuroradiol. 2013;19(2):250-253. doi:10.1177/159101991301900217
48. Stewart AF. Clinical practice. Hypercalcemia associated with cancer. N Engl J Med. 2005;352(4):373-379. doi:10.1056/NEJMcp042806
49. Vitiello R, Bellieni A, Oliva MS, et al. The importance of geriatric and surgical co-management of elderly in muscoloskeletal oncology: A literature review. Orthop Rev (Pavia). 2020;12(Suppl 1):8662. doi:10.4081/or.2020.8662
50. Heindel W, Gübitz R, Vieth V, Weckesser M, Schober O, Schäfers M. The diagnostic imaging of bone metastases. Dtsch Arztebl Int. 2014;111(44):741-747. doi:10.3238/arztebl.2014.0741
51. Rybak LD, Rosenthal DI. Radiological imaging for the diagnosis of bone metastases. Q J Nucl Med. 2001;45(1):53-64.
52. Hamaoka T, Madewell JE, Podoloff DA, Hortobagyi GN, Ueno NT. Bone imaging in metastatic breast cancer. J Clin Oncol. 2004;22(14):2942-2953. doi:10.1200/JCO.2004.08.181
53. Higinbotham NL, Marcove RC. The management of pathological fractures. J Trauma. 1965;5(6):792-798. doi:10.1097/00005373-196511000-00015
54. Yang H-L, Liu T, Wang X-M, Xu Y, Deng S-M. Diagnosis of bone metastases: a meta-analysis comparing 18FDG PET, CT, MRI and bone scintigraphy. Eur Radiol. 2011;21(12):2604-2617. doi:10.1007/s00330-011-2221-4
55. Piccardo A, Altrinetti V, Bacigalupo L, et al. Detection of metastatic bone lesions in breast cancer patients: fused (18)F-Fluoride-PET/MDCT has higher accuracy than MDCT. Preliminary experience. Eur J Radiol. 2012;81(10):2632-2638. doi:10.1016/j.ejrad.2011.12.020
56. Qu X, Huang X, Yan W, Wu L, Dai K. A meta-analysis of 18FDG-PET-CT, 18FDG-PET, MRI and bone scintigraphy for diagnosis of bone metastases in patients with lung cancer. Eur J Radiol. 2012;81(5):1007-1015. doi:10.1016/j.ejrad.2011.01.126
57. Perisano C, Spinelli MS, Graci C, et al. Soft tissue metastases in lung cancer: a review of the literature. Eur Rev Med Pharmacol Sci. 2012;16(14):1908-1914.
58. Tamburrelli FC, Meluzio MC, Masci G, Perna A, Burrofato A, Proietti L. Etiopathogenesis of Traumatic Spinal Epidural Hematoma. Neurospine. 2018;15(1):101-107. doi:10.14245/ns.1834938.469
59. Lardinois D, Weder W, Hany TF, et al. Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography. N Engl J Med. 2003;348(25):2500-2507. doi:10.1056/NEJMoa022136
60. Huellner MW, de Galiza Barbosa F, Husmann L, et al. TNM Staging of Non-Small Cell Lung Cancer: Comparison of PET/MR and PET/CT. J Nucl Med. 2016;57(1):21-26. doi:10.2967/jnumed.115.162040
61. Silvestri GA, Gonzalez AV, Jantz MA, et al. Methods for staging non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143(5 Suppl):e211S-e250S. doi:10.1378/chest.12-2355
62. Ettinger DS, Wood DE, Akerley W, et al. Non-small cell lung cancer, version 1.2015. J Natl Compr Canc Netw. 2014;12(12):1738-1761. doi:10.6004/jnccn.2014.0176
63. Chang M-C, Chen J-H, Liang J-A, et al. Meta-analysis: comparison of F-18 fluorodeoxyglucose-positron emission tomography and bone scintigraphy in the detection of bone metastasis in patients with lung cancer. Acad Radiol. 2012;19(3):349-357. doi:10.1016/j.acra.2011.10.018
64. Silva GT, Silva LM, Bergmann A, Thuler LC. Bone metastases and skeletal-related events: incidence and prognosis according to histological subtype of lung cancer. Future Oncol. 2019;15(5):485-494. doi:10.2217/fon-2018-0613
65. Fallon M, Giusti R, Aielli F, et al. Management of cancer pain in adult patients: ESMO Clinical Practice Guidelines. Ann Oncol. 2018;29 Suppl 4:iv166-iv191. doi:10.1093/annonc/mdy152
66. Zajączkowska R, Kocot-Kępska M, Leppert W, Wordliczek J. Bone Pain in Cancer Patients: Mechanisms and Current Treatment. Int J Mol Sci. 2019;20(23). doi:10.3390/ijms20236047
67. D’Oronzo S, Coleman R, Brown J, Silvestris F. Metastatic bone disease: Pathogenesis and therapeutic options: Up-date on bone metastasis management. J Bone Oncol. 2019;15:004-004. doi:10.1016/j.jbo.2018.10.004
68. Sousa S, Clézardin P. Bone-Targeted Therapies in Cancer-Induced Bone Disease. Calcif Tissue Int. 2018;102(2):227-250. doi:10.1007/s00223-017-0353-5
69. Roelofs AJ, Thompson K, Ebetino FH, Rogers MJ, Coxon FP. Bisphosphonates: molecular mechanisms of action and effects on bone cells, monocytes and macrophages. Curr Pharm Des. 2010;16(27):2950-2960. doi:10.2174/138161210793563635
70. Naoe M, Ogawa Y, Takeshita K, et al. Zoledronate stimulates gamma delta T cells in prostate cancer patients. Oncol Res. 2010;18(10):493-501. doi:10.3727/096504010x12671222663638
71. Coleman R, Body JJ, Aapro M, Hadji P, Herrstedt J, ESMO Guidelines Working Group. Bone health in cancer patients: ESMO Clinical Practice Guidelines. Ann Oncol. 2014;25 Suppl 3:iii124-137. doi:10.1093/annonc/mdu103
72. Henry DH, Costa L, Goldwasser F, et al. Randomized, double-blind study of denosumab versus zoledronic acid in the treatment of bone metastases in patients with advanced cancer (excluding breast and prostate cancer) or multiple myeloma. J Clin Oncol. 2011;29(9):1125-1132. doi:10.1200/JCO.2010.31.3304
73. De Felice F, Piccioli A, Musio D, Tombolini V. The role of radiation therapy in bone metastases management. Oncotarget. 2017;8(15):25691-25699. doi:10.18632/oncotarget.14823
74. Hartsell WF, Scott CB, Bruner DW, et al. Randomized trial of short- versus long-course radiotherapy for palliation of painful bone metastases. J Natl Cancer Inst. 2005;97(11):798-804. doi:10.1093/jnci/dji139
75. Foro Arnalot P, Fontanals AV, Galcerán JC, et al. Randomized clinical trial with two palliative radiotherapy regimens in painful bone metastases: 30 Gy in 10 fractions compared with 8 Gy in single fraction. Radiother Oncol. 2008;89(2):150-155. doi:10.1016/j.radonc.2008.05.018
76. Lutz S. The role of radiation therapy in controlling painful bone metastases. Curr Pain Headache Rep. 2012;16(4):300-306. doi:10.1007/s11916-012-0271-1
77. Goblirsch MJ, Zwolak PP, Clohisy DR. Biology of bone cancer pain. Clin Cancer Res. 2006;12(20 Pt 2):6231s-6235s. doi:10.1158/1078-0432.CCR-06-0682
78. Steenland E, Leer JW, van Houwelingen H, et al. The effect of a single fraction compared to multiple fractions on painful bone metastases: a global analysis of the Dutch Bone Metastasis Study. Radiother Oncol. 1999;52(2):101-109. doi:10.1016/s0167-8140(99)00110-3
79. Chen AB, Cronin A, Weeks JC, et al. Palliative radiation therapy practice in patients with metastatic non-small-cell lung cancer: a Cancer Care Outcomes Research and Surveillance Consortium (CanCORS) Study. J Clin Oncol. 2013;31(5):558-564. doi:10.1200/jco.2012.43.7954
80. Fairchild A. Palliative radiotherapy for bone metastases from lung cancer: Evidence-based medicine? World J Clin Oncol. 2014;5(5):845-857. doi:10.5306/wjco.v5.i5.845
81. Patchell RA, Tibbs PA, Regine WF, et al. Direct decompressive surgical resection in the treatment of spinal cord compression caused by metastatic cancer: a randomised trial. Lancet. 2005;366(9486):643-648. doi:10.1016/S0140-6736(05)66954-1
82. George R, Jeba J, Ramkumar G, Chacko AG, Tharyan P. Interventions for the treatment of metastatic extradural spinal cord compression in adults. Cochrane Database Syst Rev. 2015;(9):CD006716. doi:10.1002/14651858.CD006716.pub3
83. Chow E, Zeng L, Salvo N, Dennis K, Tsao M, Lutz S. Update on the systematic review of palliative radiotherapy trials for bone metastases. Clin Oncol (R Coll Radiol). 2012;24(2):112-124. doi:10.1016/j.clon.2011.11.004
84. Brodowicz T, O’Byrne K, Manegold C. Bone matters in lung cancer. Ann Oncol. 2012;23(9):2215-2222. doi:10.1093/annonc/mds009
85. Böhm P, Huber J. The surgical treatment of bony metastases of the spine and limbs. J Bone Joint Surg Br. 2002;84(4):521-529. doi:10.1302/0301-620x.84b4.12495
86. Chandrasekar CR, Grimer RJ, Carter SR, Tillman RM, Abudu A, Buckley L. Modular endoprosthetic replacement for tumours of the proximal femur. J Bone Joint Surg Br. 2009;91(1):108-112. doi:10.1302/0301-620X.91B1.20448
87. Talbot M, Turcotte RE, Isler M, Normandin D, Iannuzzi D, Downer P. Function and health status in surgically treated bone metastases. Clin Orthop Relat Res. 2005;438:215-220. doi:10.1097/01.blo.0000170721.07088.2e
88. Nooh A, Goulding K, Isler MH, et al. Early Improvement in Pain and Functional Outcome but Not Quality of Life After Surgery for Metastatic Long Bone Disease. Clin Orthop Relat Res. 2018;476(3):535-545. doi:10.1007/s11999.0000000000000065
89. Piccioli A, Ventura A, Maccauro G, Spinelli MS, Del Bravo V, Rosa MA. Local adjuvants in surgical management of bone metastases. Int J Immunopathol Pharmacol. 2011;24(1 Suppl 2):129-132. doi:10.1177/03946320110241S224
90. Mirels H. Metastatic disease in long bones: A proposed scoring system for diagnosing impending pathologic fractures. 1989. Clin Orthop Relat Res. 2003;(415 Suppl):S4-13. doi:10.1097/01.blo.0000093045.56370.dd
91. Howard EL, Shepherd KL, Cribb G, Cool P. The validity of the Mirels score for predicting impending pathological fractures of the lower limb. Bone Joint J. 2018;100-B(8):1100-1105. doi:10.1302/0301-620X.100B8.BJJ-2018-0300.R1
92. Errani C, Mavrogenis AF, Cevolani L, et al. Treatment for long bone metastases based on a systematic literature review. Eur J Orthop Surg Traumatol. 2017;27(2):205-211. doi:10.1007/s00590-016-1857-9
93. Capanna R, Piccioli A, Di Martino A, et al. Management of long bone metastases: recommendations from the Italian Orthopaedic Society bone metastasis study group. Expert Rev Anticancer Ther. 2014;14(10):1127-1134. doi:10.1586/14737140.2014.947691
94. Steensma M, Healey JH. Trends in the surgical treatment of pathologic proximal femur fractures among Musculoskeletal Tumor Society members. Clin Orthop Relat Res. 2013;471(6):2000-2006. doi:10.1007/s11999-012-2724-6
95. Jacofsky DJ, Haidukewych GJ. Management of pathologic fractures of the proximal femur: state of the art. J Orthop Trauma. 2004;18(7):459-469. doi:10.1097/00005131-200408000-00013
96. Steensma M, Boland PJ, Morris CD, Athanasian E, Healey JH. Endoprosthetic treatment is more durable for pathologic proximal femur fractures. Clin Orthop Relat Res. 2012;470(3):920-926. doi:10.1007/s11999-011-2047-z
97. Harvey N, Ahlmann ER, Allison DC, Wang L, Menendez LR. Endoprostheses last longer than intramedullary devices in proximal femur metastases. Clin Orthop Relat Res. 2012;470(3):684-691. doi:10.1007/s11999-011-2038-0
98. Potter BK, Chow VE, Adams SC, Letson GD, Temple HT. Endoprosthetic proximal femur replacement: metastatic versus primary tumors. Surg Oncol. 2009;18(4):343-349. doi:10.1016/j.suronc.2008.08.007
99. Meynard P, Seguineau A, Laumonerie P, et al. Surgical management of proximal femoral metastasis: Fixation or hip replacement? A 309 case series. Orthop Traumatol Surg Res. 2020;106(6):1013-1023. doi:10.1016/j.otsr.2020.05.007
100. Healey JH, Shannon F, Boland P, DiResta GR. PMMA to stabilize bone and deliver antineoplastic and antiresorptive agents. Clin Orthop Relat Res. 2003;(415 Suppl):S263-275. doi:10.1097/01.blo.0000093053.96273.ee
101. Piccioli A, Rossi B, Scaramuzzo L, Spinelli MS, Yang Z, Maccauro G. Intramedullary nailing for treatment of pathologic femoral fractures due to metastases. Injury. 2014;45(2):412-417. doi:10.1016/j.injury.2013.09.025
102. Vles GF, Brodermann MH, Roussot MA, Youngman J. Carbon-Fiber-Reinforced PEEK Intramedullary Nails Defining the Niche. Case Rep Orthop. 2019;2019:1538158. doi:10.1155/2019/1538158
103. Spinelli MS, Ziranu A, Piccioli A, Maccauro G. Surgical treatment of acetabular metastasis. Eur Rev Med Pharmacol Sci. 2016;20(14):3005-3010.
104. 2.15 Pathological pelvic fractures and acetabular reconstruction in metastatic disease. In: Fractures of the Pelvis and Acetabulum. Fourth Edition. Thieme Verlag; 2015. doi:10.1055/b-0035-121667
105. Cotten A, Deprez X, Migaud H, Chabanne B, Duquesnoy B, Chastanet P. Malignant acetabular osteolyses: percutaneous injection of acrylic bone cement. Radiology. 1995;197(1):307-310. doi:10.1148/radiology.197.1.7568843
106. Scaramuzzo L, Maccauro G, Rossi B, Messuti L, Maffulli N, Logroscino CA. Quality of life in patients following percutaneous PMMA acetabuloplasty for acetabular metastasis due to carcinoma. Acta Orthop Belg. 2009;75(4):484-489.
107. Tillman RM, Myers GJC, Abudu AT, Carter SR, Grimer RJ. The three-pin modified “Harrington” procedure for advanced metastatic destruction of the acetabulum. J Bone Joint Surg Br. 2008;90(1):84-87. doi:10.1302/0301-620X.90B1.19892
108. Parikh SN, Kreder HJ. Pelvic reconstruction for massive acetabular insufficiency. Clin Orthop Relat Res. 2005;(434):217-221. doi:10.1097/01.blo.0000155077.44851.45
109. Kitagawa Y, Ek ET, Choong PFM. Pelvic reconstruction using saddle prosthesis following limb salvage operation for periacetabular tumour. J Orthop Surg (Hong Kong). 2006;14(2):155-162. doi:10.1177/230949900601400210
110. Joaquim AF, Powers A, Laufer I, Bilsky MH. An update in the management of spinal metastases. Arq Neuropsiquiatr. 2015;73(9):795-802. doi:10.1590/0004-282X20150099
111. Tomita K, Kawahara N, Kobayashi T, Yoshida A, Murakami H, Akamaru T. Surgical strategy for spinal metastases. Spine (Phila Pa 1976). 2001;26(3):298-306. doi:10.1097/00007632-200102010-00016
112. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol. 2008;61(10):991-996. doi:10.1016/j.jclinepi.2007.11.010
113. Bartels RHMA, van der Linden YM, van der Graaf WTA. Spinal extradural metastasis: review of current treatment options. CA Cancer J Clin. 2008;58(4):245-259. doi:10.3322/CA.2007.0016
114. Fourney DR, Schomer DF, Nader R, et al. Percutaneous vertebroplasty and kyphoplasty for painful vertebral body fractures in cancer patients. J Neurosurg. 2003;98(1 Suppl):21-30. doi:10.3171/spi.2003.98.1.0021
115. Wenger M. Vertebroplasty for metastasis. Med Oncol. 2003;20(3):203-209. doi:10.1385/MO:20:3:203
116. Masala S, Anselmetti GC, Muto M, Mammucari M, Volpi T, Simonetti G. Percutaneous vertebroplasty relieves pain in metastatic cervical fractures. Clin Orthop Relat Res. 2011;469(3):715-722. doi:10.1007/s11999-010-1550-y
117. Axelsen M, Thomassen LD, Bünger C, et al. Estimating risk of pulmonary neoplastic embolism during vertebroplasty. Spine (Phila Pa 1976). 2012;37(7):551-556. doi:10.1097/BRS.0b013e31822e7a98
118. Hirabayashi H, Ebara S, Kinoshita T, et al. Clinical outcome and survival after palliative surgery for spinal metastases: palliative surgery in spinal metastases. Cancer. 2003;97(2):476-484. doi:10.1002/cncr.11039
119. Uei H, Tokuhashi Y, Oshima M, et al. Clinical Results of Minimally Invasive Spine Stabilization for Spinal Metastases. Orthopedics. 2017;40(4):e693-e698. doi:10.3928/01477447-20170522-02
120. Hansen-Algenstaedt N, Kwan MK, Algenstaedt P, et al. Comparison Between Minimally Invasive Surgery and Conventional Open Surgery for Patients With Spinal Metastasis: A Prospective Propensity Score-Matched Study. Spine (Phila Pa 1976). 2017;42(10):789-797. doi:10.1097/BRS.0000000000001893
121. Uei H, Tokuhashi Y, Maseda M, et al. Comparison between minimally invasive spine stabilization with and without posterior decompression for the management of spinal metastases: a retrospective cohort study. J Orthop Surg Res. 2018;13. doi:10.1186/s13018-018-0777-2
122. Capanna R, De Biase P, Sensi L. [Minimally invasive techniques for treatment of metastatic cancer]. Orthopade. 2009;38(4):343-347. doi:10.1007/s00132-008-1378-2
123. Carrafiello G, Laganà D, Pellegrino C, et al. Ablation of painful metastatic bone tumors: a systematic review. Int J Surg. 2008;6 Suppl 1:S47-52. doi:10.1016/j.ijsu.2008.12.035
124. Choi J, Raghavan M. Diagnostic imaging and image-guided therapy of skeletal metastases. Cancer Control. 2012;19(2):102-112. doi:10.1177/107327481201900204
125. Callstrom MR, Charboneau JW, Goetz MP, et al. Image-guided ablation of painful metastatic bone tumors: a new and effective approach to a difficult problem. Skeletal Radiol. 2006;35(1):1-15. doi:10.1007/s00256-005-0003-2
126. Simon MA, Finn HA. Diagnostic strategy for bone and soft-tissue tumors. Instr Course Lect. 1994;43:527-536.
127. Harrington KD, Sim FH, Enis JE, Johnston JO, Diok HM, Gristina AG. Methylmethacrylate as an adjunct in internal fixation of pathological fractures. Experience with three hundred and seventy-five cases. J Bone Joint Surg Am. 1976;58(8):1047-1055.
128. Healey JH, Brown HK. Complications of bone metastases: surgical management. Cancer. 2000;88(12 Suppl):2940-2951. doi:10.1002/1097-0142(20000615)88:12+<2940::aid-cncr10>3.0.co;2-w
129. Bonnevialle P, Baron-Trocellier T, Niglis L, et al. Functional results and survival after surgery for peripheral skeletal metastasis: A 434-case multicenter retrospective series. Orthop Traumatol Surg Res. 2020;106(6):997-1003. doi:10.1016/j.otsr.2019.10.024
130. Armstrong V, Schoen N, Madhavan K, Vanni S. A systematic review of interventions and outcomes in lung cancer metastases to the spine. J Clin Neurosci. 2019;62:66-71. doi:10.1016/j.jocn.2019.01.006
131. Capanna R, Campanacci DA. The treatment of metastases in the appendicular skeleton. J Bone Joint Surg Br. 2001;83(4):471-481. doi:10.1302/0301-620x.83b4.12202
132. Kopacz J, Mazurkiewicz T, Warda E. Complications after surgical treatment of bone metastases to proximal femur. Ortop Traumatol Rehabil. 2003;5(3):313-318.
133. Thai DM, Kitagawa Y, Choong PF. Outcome of surgical management of bony metastases to the humerus and shoulder girdle: a retrospective analysis of 93 patients. Int Semin Surg Oncol. 2006;3:5. doi:10.1186/1477-7800-3-5
134. Piccioli A, Donati F, Giacomo GD, et al. Infective complications in tumour endoprostheses implanted after pathological fracture of the limbs. Injury. 2016;47 Suppl 4:S22-S28. doi:10.1016/j.injury.2016.07.054
135. El Ezzo O, Oliva MS, Cauteruccio M, et al. Innovations in prevention of infections in oncological megaprostheses: a narrative review. J Biol Regul Homeost Agents. 2020;34(4 Suppl. 3):275-278. Congress of the Italian Orthopaedic Research Society.
136. Donati F, Di Giacomo G, Ziranu A, et al. SILVER COATED PROSTHESIS IN ONCOLOGICAL LIMB SALVAGE SURGERY REDUCE THE INFECTION RATE. J Biol Regul Homeost Agents. 2015;29(4 Suppl):149-155.
137. Cook RJ, Major P. Multistate analysis of skeletal events in patients with bone metastases. Clin Cancer Res. 2006;12(20 Pt 2):6264s-6269s. doi:10.1158/1078-0432.CCR-06-0654
138. Ogihara S, Seichi A, Hozumi T, et al. Prognostic factors for patients with spinal metastases from lung cancer. Spine (Phila Pa 1976). 2006;31(14):1585-1590. doi:10.1097/01.brs.0000222146.91398.c9
139. Zhang L, Gong Z. Clinical Characteristics and Prognostic Factors in Bone Metastases from Lung Cancer. Med Sci Monit. 2017;23:4087-4094. doi:10.12659/msm.902971
140. Kadota K, Sima CS, Arcila ME, et al. KRAS Mutation Is a Significant Prognostic Factor in Early-stage Lung Adenocarcinoma. Am J Surg Pathol. 2016;40(12):1579-1590. doi:10.1097/PAS.0000000000000744
141. Selvaggi G, Scagliotti GV. Management of bone metastases in cancer: a review. Crit Rev Oncol Hematol. 2005;56(3):365-378. doi:10.1016/j.critrevonc.2005.03.011
142. Rades D, Haus R, Janssen S, Schild SE. An easy-to-use scoring system to estimate the survival of patients irradiated for bone metastases from lung cancer. Transl Lung Cancer Res. 2020;9(4):1067-1073. doi:10.21037/tlcr-19-642
143. Svensson E, Christiansen CF, Ulrichsen SP, Rørth MR, Sørensen HT. Survival after bone metastasis by primary cancer type: a Danish population-based cohort study. BMJ Open. 2017;7(9):e016022. doi:10.1136/bmjopen-2017-016022