Chinese clinical guidelines on diagnosis and treatment of lung cancer bone metastasis (version 2024)_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

 ZHI Xiuyi ¹ ,  WANG Jie ² ,  LIU Lunxu ³ ,  ZHAO Jun ⁴ , Lung Cancer Medical Education Committee of Chinese Medicine Education Association, Youth Expert Committee on Lung Cancer of Beijing Medical Award Foundation , Lung Cancer Professional Committee of China Geriatric Health Association

1. Department of Thoracic Surgery, Xuanwu Hospital, Capital Medical University, Beijing, 100053, P. R. China;
2. Department of Oncology, Cancer Hospital, Chinese Academy of Medical Sciences, Beijing, 100021, P. R. China;
3. Department of Thoracic Surgery, West China Hospital of Sichuan University, Chengdu, 610041, P. R. China;
4. Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department 1 of Thoracic Oncology, Peking University Cancer Hospital and Institute, Beijing, 100142, P. R. China;

Corresponding author：

ZHI Xiuyi, Email: xiuyizhi2015@163.com; WANG Jie, Email: wangjie_cc@yahoo.com; LIU Lunxu, Email: lunxu_liu@aliyun.com; ZHAO Jun, Email: ohjerry@163.com

Keywords：

Lung cancer; bone metastasis; bone-modifying therapy; clinical guideline; recommendations

DOI：

10.7507/1007-4848.202402042

Video：

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Lung cancer is the highest morbidity of malignant tumor in China, and bone metastasis is one of the common sites. With the development of imaging and nuclear medicine technology, the level of early diagnosis of bone metastasis has been improved. There are also many evidence-based evidences and advances in systemic therapy (chemotherapy, targeted therapy, immunotherapy) and bone modification drugs for treatment of bone metastases from lung cancer. The comprehensive treatment model under the guidance of multiple disciplines (including medical oncology, surgery, radiotherapy, interventional medicine, nuclear medicine, psychological rehabilitation, etc.) has been widely implemented in clinical practice. Therefore, Lung Cancer Medical Education Committee of China Medicine Education Association, Youth Specialists Committee of Lung Cancer, Beijing Medical Award Foundation and Lung Cancer Specialty Committee of Chinese Elderly Health Care Association have written the "Chinese Clinical Guidelines on Diagnosis and Treatment of Lung Cancer Bone Metastasis (Version 2024)", based on the "Expert Consensus on Diagnosis and Treatment of Lung Cancer Bone Metastasis (Version 2019)". The aim is to enhance the comprehensive treatment level of lung cancer bone metastasis in China.

Citation： ZHI Xiuyi, WANG Jie, LIU Lunxu, ZHAO Jun, Lung Cancer Medical Education Committee of Chinese Medicine Education Association, Youth Expert Committee on Lung Cancer of Beijing Medical Award Foundation, Lung Cancer Professional Committee of China Geriatric Health Association. Chinese clinical guidelines on diagnosis and treatment of lung cancer bone metastasis (version 2024). Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(5): 643-654. doi: 10.7507/1007-4848.202402042 Copy

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1. Hong S, Youk T, Lee SJ, et al. Bone metastasis and skeletal-related events in patients with solid cancer: A Korean nationwide health insurance database study. PLoS One, 2020, 15(7): e0234927.
2. Guo X, Ma W, Wu H, et al. Synchronous bone metastasis in lung cancer: Retrospective study of a single center of 15, 716 patients from Tianjin, China. BMC Cancer, 2021, 21(1): 613.
3. Nakahara Y, Hosomi Y, Shibuya M, et al. Multicenter study of zoledronic acid administration in non-small-cell lung cancer patients with bone metastasis: Thoracic oncology research group (TORG) 1017. Mol Clin Oncol, 2019, 11(4): 349-353.
4. 董智, 赵军, 柳晨,等. 肺癌骨转移诊疗专家共识(2019版). 中国肺癌杂志, 2019, 22(4): 187-207.
5. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: An emerging consensus on rating quality of evidence and strength of recommendations. BMJ, 2008, 336(7650): 924-926.
6. Okamoto K. Role of RANKL in cancer development and metastasis. J Bone Miner Metab, 2021, 39(1): 71-81.
7. Li B, Wang P, Jiao J, et al. Roles of the RANKL-RANK axis in immunity-implications for pathogenesis and treatment of bone metastasis. Front Immunol, 2022, 13: 824117.
8. Qu X, Huang X, Yan W, et al. 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.
9. D'Addario G, Felip E, ESMO Guidelines Working Group. Non-small-cell lung cancer: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol, 2009, 20 Suppl 4: 68-70.
10. Liu T, Cheng T, Xu W, et al. A meta-analysis of ¹⁸FDG-PET, MRI and bone scintigraphy for diagnosis of bone metastases in patients with breast cancer. Skeletal Radiol, 2011, 40(5): 523-531.
11. Zhi XY, Wu YL, Bu H, et al. Chinese guidelines on the diagnosis and treatment of primary lung cancer (2011). J Thorac Dis, 2012, 4(1): 88-101.
12. 江泽飞, 宋三泰, 于世英, 等. 乳腺癌骨转移和骨相关疾病临床诊疗专家共识(2008版). 中华肿瘤杂志, 2009, 31(2): 156-159.
13. Yang HL, Liu T, Wang XM, et al. Diagnosis of bone metastases: A meta-analysis comparing ¹⁸FDG PET, CT, MRI and bone scintigraphy. Eur Radiol, 2011, 21(12): 2604-2617.
14. Dong Y, Zheng S, Machida H, et al. Differential diagnosis of osteoblastic metastases from bone islands in patients with lung cancer by single-source dual-energy CT: Advantages of spectral CT imaging. Eur J Radiol, 2015, 84(5): 901-907.
15. Luo H, Zou L, Yang Q, et al. Spectral CT assists differentiation of osteoblastic bone metastasis from bone island in newly diagnosed cancer patients. Eur Radiol, 2024, 34(1): 60-68.
16. Shao G, Gu W, Guo M, et al. Clinical study of ⁹⁹mTc-3P-RGD2 peptide imaging in osteolytic bone metastasis. Oncotarget, 2017, 8(43): 75587-75596.
17. Daldrup-Link HE, Franzius C, Link TM, et al. Whole-body MR imaging for detection of bone metastases in children and young adults: Comparison with skeletal scintigraphy and FDG PET. AJR Am J Roentgenol, 2001, 177(1): 229-236.
18. Hamaoka T, Madewell JE, Podoloff DA, et al. Bone imaging in metastatic breast cancer. J Clin Oncol, 2004, 22(14): 2942-2953.
19. Schmidt GP, Schoenberg SO, Reiser MF, et al. Whole-body MR imaging of bone marrow. Eur J Radiol, 2005, 55(1): 33-40.
20. Li EC, Davis LE. Zoledronic acid: A new parenteral bisphosphonate. Clin Ther, 2003, 25(11): 2669-2708.
21. Lopez-Olivo MA, Shah NA, Pratt G, et al. Bisphosphonates in the treatment of patients with lung cancer and metastatic bone disease: A systematic review and meta-analysis. Support Care Cancer, 2012, 20(11): 2985-2998.
22. Saba N, Khuri F. The role of bisphosphonates in the management of advanced cancer with a focus on non-small-cell lung cancer. Part 1: Mechanisms of action, role of biomarkers and preclinical applications. Oncol, 2005, 68(1): 10-17.
23. 游如旭, 张聪, 张玉. 骨质疏松症治疗药物合理应用专家共识(2023). 中国医院药学杂志, 2024, URL: http://kns.cnki.net/kcms/detail/42.1204.R.20240226.0954.006.html.
24. Jiang Z, Shao Z, Zhang Q, et al. Efficacy and safety of denosumab from a phase Ⅲ, randomized, active-controlled study compared with zoledronic acid in patients of asian ancestry with bone metastases from solid tumors. JCO, 2016, 34(15_suppl): 10116-10116.
25. 李中梨, 王剑锋, 张文学. 因卡膦酸二钠与唑来膦酸治疗癌性骨转移性疼痛的疗效比较. 肿瘤综合治疗电子杂志, 2020, 6(1): 115-117.
26. 中国抗癌协会泌尿男生殖系统肿瘤专业委员会. 肾癌骨转移临床诊疗专家共识(2021版). 中华肿瘤杂志, 2021, 43(10): 1007-1015.
27. 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. JCO, 2011, 29(9): 1125-1132.
28. Henry D, Vadhan-Raj S, Hirsh V, et al. Delaying skeletal-related events in a randomized phase 3 study of denosumab versus zoledronic acid in patients with advanced cancer: An analysis of data from patients with solid tumors. Support Care Cancer, 2014, 22(3): 679-687.
29. Lipton A, Fizazi K, Stopeck AT, et al. Superiority of denosumab to zoledronic acid for prevention of skeletal-related events: A combined analysis of 3 pivotal, randomised, phase 3 trials. Eur J Cancer, 2012, 48(16): 3082-3092.
30. Fizazi K, Lipton A, Mariette X, et al. Randomized phase Ⅱ trial of denosumab in patients with bone metastases from prostate cancer, breast cancer, or other neoplasms after intravenous bisphosphonates. J Clin Oncol, 2009, 27(10): 1564-1571.
31. Martin M, Bell R, Bourgeois H, et al. Bone-related complications and quality of life in advanced breast cancer: Results from a randomized phase Ⅲtrial of denosumab versus zoledronic acid. Clin Cancer Res, 2012, 18(17): 4841-4849.
32. Niu X, Wei F, Tu C, et al. Efficacy and safety of JMT103 in patients with giant cell tumor of bone: A multicenter, single-arm, open-label, phase Ⅰb/Ⅱ study. JCO, 2021, 39(15_suppl): 11526-11526.
33. Mancini I, Dumon JC, Body JJ. Efficacy and safety of ibandronate in the treatment of opioid-resistant bone pain associated with metastatic bone disease: A pilot study. J Clin Oncol, 2004, 22(17): 3587-3592.
34. Ross JR, Saunders Y, Edmonds PM, et al. Systematic review of role of bisphosphonates on skeletal morbidity in metastatic cancer. BMJ, 2003, 327(7413): 469.
35. Ng TL, Tu MM, Ibrahim MFK, et al. Long-term impact of bone-modifying agents for the treatment of bone metastases: A systematic review. Support Care Cancer, 2021, 29(2): 925-943.
36. Anderson K, Ismaila N, Kyle RA. Role of bone-modifying agents in multiple myeloma: American Society of Clinical Oncology clinical practice guideline update summary. JOP, 2018, 14(4): 266-269.
37. Stopeck AT, Lipton A, Body JJ, et al. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: A randomized, double-blind study. J Clin Oncol, 2010, 28(35): 5132-5139.
38. Fizazi K, Carducci M, Smith M, et al. Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: A randomised, double-blind study. Lancet, 2011, 377(9768): 813-822.
39. Katsarelis H, Shah NP, Dhariwal DK, et al. Infection and medication-related osteonecrosis of the jaw. J Dent Res, 2015, 94(4): 534-539.
40. Zhang C, Shen G, Li H, et al. Incidence rate of osteonecrosis of jaw after cancer treated with bisphosphonates and denosumab: A systematic review and meta-analysis. Spec Care Dentist, 2024, 44(2): 530-541.
41. Van Poznak CH, Unger JM, Darke AK, et al. Association of osteonecrosis of the jaw with zoledronic acid treatment for bone metastases in patients with cancer. JAMA Oncol, 2021, 7(2): 246-254.
42. Zuradelli M, Masci G, Biancofiore G, et al. High incidence of hypocalcemia and serum creatinine increase in patients with bone metastases treated with zoledronic acid. Oncologist, 2009, 14(5): 548-556.
43. Body JJ, Bone HG, de Boer RH, et al. Hypocalcaemia in patients with metastatic bone disease treated with denosumab. Eur J Cancer, 2015, 51(13): 1812-1821.
44. Nistor CE, Ciuche A, Cucu AP, et al. Management of lung cancer presenting with solitary bone metastasis. Medicina (Kaunas), 2022, 58(10): 1463.
45. Landi L, D'Incà F, Gelibter A, et al. Bone metastases and immunotherapy in patients with advanced non-small-cell lung cancer. J Immunother Cancer, 2019, 7(1): 316.
46. Huang Y, Zhu L, Guo T, et al. Metastatic sites as predictors in advanced NSCLC treated with PD-1 inhibitors: A systematic review and meta-analysis. Hum Vaccin Immunother, 2021, 17(5): 1278-1287.
47. Li X, Wang L, Chen S, et al. Adverse impact of bone metastases on clinical outcomes of patients with advanced non-small cell lung cancer treated with immune checkpoint inhibitors. Thorac Cancer, 2020, 11(10): 2812-2819.
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Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Chinese clinical guidelines on diagnosis and treatment of lung cancer bone metastasis (version 2024)

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