Research progress and prospect of molecular mechanism, biomarkers and treatment of bone metastasis in lung cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

ZHOU Pengfei ¹ ,  ZHOU Jie ² , ZHANG Hongwei ¹

1. Department of Thoracic Oncology, Meishan Cancer Hospital, Meishan, 620020, Sichuan, P. R. China;
2. Department of Radiation Oncology, Radiation Oncology Key Laboratory of Sichuan Province, Sichuan Clinical Research Center for Cancer, Sichuan Cancer Hospital & Institute, Sichuan Cancer Center, University of Electronic Science and Technology of China, Chengdu, 610041, P. R. China;

Corresponding author：

ZHOU Jie, Email: zjoncology2023@163.com

Keywords：

Lung cancer; bone metastasis; biomarkers; molecular mechanism; treatment; progress; review

DOI：

10.7507/1007-4848.202504088

Video：

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[Abstract] Bone metastasis is one of the common complications of lung cancer, which seriously affects the quality of life and survival of patients. At present, the clinical diagnosis of bone metastasis of lung cancer mainly depends on imaging methods, but due to its lack of sensitivity and potential radiation risk, about half of patients have already had bone-related events when they are diagnosed clearly. The treatment of bone metastasis of lung cancer mainly depends on surgery, radiotherapy and chemotherapy, targeted therapy, immunosuppressants, etc. Although the treatment of bone metastasis of lung cancer has made some progress in recent years, there are still some problems such as high risk of other distant metastasis. This article mainly reviews the pathogenesis, diagnostic biomarkers and treatment progress of bone metastasis of lung cancer, in order to provide reference for the diagnosis and treatment of bone metastasis of lung cancer.

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2.	Ye WL, Zhao YP, Cheng Y, et al. Bone metastasis target redox-responsive micell for the treatment of lung cancer bone metastasis and anti-bone resorption. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 380-391.
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5.	白娟, 蒲萍, 郑玲. 小细胞肺癌发生骨转移及骨相关事件的风险因素分析. 现代肿瘤医学, 2019, 27(16): 2876-2879.Bai J, Pu P, Zheng L. Risk factors of bone metastasis and bone-related events in small cell lung cancer. Modern Oncol, 2019, 27(16): 2876-2879.
6.	Gao Y, Wu M, Rizvi SAA, et al. Exploring the key pathogenic mechanisms and potential intervention targets for Sophorae Flavescentis radix in managing bone metastasis of lung cancer based on network pharmacology and molecular docking techniques. Transl Cancer Res, 2024, 13(10): 5616-5626.
7.	Wu B, Zhu Y, Hu Z, et al. Machine learning predictive models and risk factors for lymph node metastasis in non-small cell lung cancer. BMC Pulm Med, 2024, 24(1): 526.
8.	Asano Y, Yamamoto N, Hayashi K, et al. Serum inflammatory dynamics as novel biomarkers for immune checkpoint inhibitors in non-small-cell lung cancer with bone metastases. Anticancer Res, 2024, 44(10): 4493-4503.
9.	Pu D, Zhang HE, Li L. Immune-related osteoblastic bone alterations mimicking bone metastasis in a small-cell lung cancer patient treated with durvalumab: a case report. Transl Lung Cancer Res, 2024, 13(8): 2043-2049.
10.	Guo Y, Lin Q, Zhao S, et al. Automated detection of lung cancer-caused metastasis by classifying scintigraphic images using convolutional neural network with residual connection and hybrid attention mechanism. Insights Imaging, 2022, 13(1): 24.
11.	Lin Z, Wang R, Zhou Y, et al. Prediction of distant metastasis and survival prediction of gastric cancer patients with metastasis to the liver, lung, bone, and brain: research based on the SEER database. Ann Transl Med, 2022, 10(1): 16.
12.	Xiaoqing H, Luopeng B, Yunyun W, et al. Genetically engineered exosomes for targetedly preventing premetastatic niche formation and suppressing postoperative melanoma lung metastasis. Nano Today, 2022, 3(1): 46.
13.	Akshaya RL, Saranya I, Salomi GM, et al. In vivo validation of the functional role of MicroRNA-4638-3p in breast cancer bone metastasis. J Cancer Res Clin Oncol, 2024, 150(2): 63.
14.	Li T, Lin Q, Guo Y, et al. Automated detection of skeletal metastasis of lung cancer with bone scans using convolutional nuclear network. Phys Med Biol, 2022, 67(1): 014001.
15.	Shi S, Wang H, Liu X, et al. Prediction of overall survival of non-small cell lung cancer with bone metastasis: an analysis of the Surveillance, Epidemiology and End Results (SEER) database. Transl Cancer Res, 2021, 10(12): 5191-5203.
16.	Hong Q, Hu H, Liu D, et al. Bioinformatic analysis of differentially expressed genes in lung cancer bone metastasis and their implications for disease progression in lung cancer patients. J Thorac Dis, 2024, 16(7): 4666-4677.
17.	Guo J, Miao J, Sun W, et al. Predicting bone metastasis-free survival in non-small cell lung cancer from preoperative CT via deep learning. NPJ Precis Oncol, 2024, 8(1): 161.
18.	Badhe PV, Sivakumar M, Lamture S, et al. White out hemithorax secondary to salivary gland type of lung cancer with metastasis in liver and bone: a case report. J Med Case Rep, 2024, 18(1): 288.
19.	Zhong N, Wang H, Zhao W, et al. High RNF7 expression enhances PD-1 resistance of non-small cell lung cancer cells by promoting CXCL1 expression and myeloid-derived suppressor cell recruitment via activating NF-κB signaling. Nan Fang Yi Ke Da Xue Xue Bao, 2024, 44(9): 1704-1711. Zhong N, Wang H, Zhao W, et al. High RNF7 expression enhances PD-1 resistance of non-small cell lung cancer cells by promoting CXCL1 expression and myeloid-derived suppressor cell recruitment via activating NF-κB signaling. J South Med Univ, 2024, 44(9): 1704-1711.
20.	Han L, Huang Z, Liu Y, et al. MicroRNA-106a regulates autophagy-related cell death and EMT by targeting TP53INP1 in lung cancer with bone metastasis. Cell Death Dis, 2021, 12(11): 1037.
21.	Lu Y, Ma J, Li Y, et al. Correction: CDP138 silencing inhibits TGF-β/Smad signaling to impair radioresistance and metastasis via GDF15 in lung cancer. Cell Death Dis, 2024, 15(7): 549.
22.	Liu G, Zhang H. ANGPT1 promotes M1 macrophage polarization and inhibits lung adenocarcinoma progression by inhibiting the TGF-β signalling pathway. Gen Physiol Biophys, 2024, 43(2): 121-138.
23.	金依诺, 汤心雨, 刘雯雯, 等. 靶向肿瘤微环境的肺癌脑转移研究进展. 中华医学杂志, 2024, 104(18): 1641-1648.Jin YN, Tang XY, Liu WW, et al. Research progress on brain metastasis of lung cancer targeting tumor microenvironment. Natl Med J China, 2024, 104(18): 1641-1648.
24.	Chen P, Min J, Wu H, et al. Annexin A1 is a potential biomarker of bone metastasis in small cell lung cancer. Oncol Lett, 2021, 21(2): 141.
25.	Liu Q, Dong Y, Ren S, et al. GPNMB associates with inferior prognosis in SCLC patients through promoting tumor cell metastasis. J Thorac Oncol, 2021, 16(10): 1194-1195.
26.	Zhang H, Zhao B, Zhai ZG, et al. Expression and clinical significance of MMP-9 and P53 in lung cancer. Eur Rev Med Pharmacol Sci, 2021, 25(3): 1358-1365.
27.	Zhang C, Zhou Y, Zhang B, et al. Identification of lncRNA, miRNA and mRNA expression profiles and ceRNA networks in small cell lung cancer. BMC Genomics, 2023, 24(1): 217.
28.	洪克林, 黄进启, 郑勇, 等. 血清CaN、COX2、TK1、Ca2+及ALP联合检测用于肺癌骨转移诊断的价值. 国际检验医学杂志, 2021, 42(4): 504-508.Hong KL, Huang JQ, Zheng Y, et al. The value of combined detection of serum CaN, COX2, TK1, Ca2+ and ALP in the diagnosis of bone metastasis of lung cancer. Int J Lab Med, 2021, 42(4): 504-508.
29.	张双捷, 王立峰. 血清ALP、PINP、PTHrP对肺癌骨转移诊断的价值. 东南大学学报(医学版), 2020, 39(3): 309-314.Zhang SJ, Wang LF. Diagnostic value of serum ALP, PINP and PTHrP for bone metastasis of lung cancer. J Southeast Univ Med Sci Ed, 2020, 39(3): 309-314.
30.	林敏, 朱柳君, 莫春香, 等. 骨代谢标志物在前列腺癌骨转移患者血清中的表达水平及其诊断价值. 广西医学, 2021, 43(9): 1074-1077.Lin M, Zhu LJ, Mo CX, et al. Expression level of bone metabolic markers in serum of patients with bone metastasis of prostate cancer and its diagnostic value. Guangxi Med J, 2021, 43(9): 1074-1077.
31.	康翠伟, 闫利鹏, 刘宁, 等. 溶骨性骨代谢标志物血Ⅰ型CTP、miR-107及TRACP-5b检测在肺癌骨转移中的诊断价值. 分子诊断与治疗杂志, 2024, 16(2): 331-334.Kang CW, Yan LP, Liu N, et al. Diagnostic value of serum type Ⅰ CTP, miR-107 and TRACP-5b as markers of osteolytic bone metabolism in bone metastasis of lung cancer. J Mol Diagn Ther, 2024, 16(2): 331-334.
32.	Congedo MT, Nachira D, Bertolaccini L, et al. Multimodal therapy for synchronous bone oligometastatic NSCLC: The role of surgery. J Surg Oncol, 2022, 125(4): 782-789.
33.	Zhu S, Ge T, Hu J, et al. Prognostic value of surgical intervention in advanced lung adenocarcinoma: a population-based study. J Thorac Dis, 2021, 13(10): 5942-5953.
34.	Sun Z, Sui X, Yang F, et al. Effects of primary tumor resection on the survival of patients with stage IV extrathoracic metastatic non-small cell lung cancer: a population-based study. Lung Cancer, 2019, 129: 98-106.
35.	郭连洪, 赵素花, 李斌, 等. 大剂量和常规分割剂量调强适形放疗联合89SrCl2静脉注射治疗肺癌骨转移的效果. 中国医学物理学杂志, 2020, 37(9): 1111-1114.Guo LH, Zhao SH, Li B, et al. Effect of high-dose and conventional fractionated dose intensity modulated radiotherapy combined with intravenous injection of 89SrCl2 on bone metastasis of lung cancer. Chin J Med Phys, 2020, 37(9): 1111-1114.
36.	徐阳, 李红云, 苏丹, 等. 伊班膦酸钠联合化疗对非小细胞肺癌骨转移患者炎性因子及骨代谢指标的影响. 实用临床医药杂志, 2022, 26(2): 52-55.Xu Y, Li HY, Su D, et al. Effects of ibandronate combined with chemotherapy on inflammatory factors and bone metabolism indexes in patients with bone metastasis from non-small cell lung cancer. J Clin Med Pract, 2022, 26(2): 52-55.
37.	Meng C, Ge X, Tian J, et al. Prognostic role of targeted therapy in patients with multiple-site metastases from non-small-cell lung cancer. Future Oncol, 2020, 16(26): 1957-1967.
38.	周艳, 邵丽丽, 王晓丽, 等. 地舒单抗联合免疫检查点抑制剂治疗实体瘤骨转移临床疗效及安全性. 现代生物医学进展, 2023, 23(13): 2563-2567,2590.Zhou Y, Shao LL, Wang XL, et al. Clinical efficacy and safety of denosumab combined with immune checkpoint inhibitor in the treatment of bone metastasis of solid tumor. Prog Mod Biomed, 2023, 23(13): 2563-2567,2590.
39.	段登科, 白智龙, 温振涛, 等. 地舒单抗治疗非小细胞肺癌骨转移临床疗效. 临床军医杂志, 2024, 52(4): 410-412.Duan DK, Bai ZL, Wen ZT, et al. Clinical effect of denosumab on bone metastasis of non-small cell lung cancer. J Clin Mil Med, 2024, 52(4): 410-412.
40.	宋飞, 向盈盈, 张纪贵, 等. 经桡动脉途径与股动脉途径介入治疗肺鳞癌的对比. 昆明医科大学学报, 2021, 42(9): 134-137.Song F, Xiang YY, Zhang JG, et al. Comparison of interventional therapy for lung squamous cell carcinoma via radial artery and femoral artery. J Kunming Med Univ, 2021, 42(9): 134-137.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Ye WL, Zhao YP, Cheng Y, et al. Bone metastasis target redox-responsive micell for the treatment of lung cancer bone metastasis and anti-bone resorption. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 380-391.
3. D'Oronzo S, Coleman R, Brown J, et al. Metastatic bone disease: pathogenesis and therapeutic options: update on bone metastasis management. J Bone Oncol, 2018, 15: 4-14.
4. So KWL, Leung EMC, Ng T, et al. Machine learning models to predict bone metastasis risk in patients with lung cancer. Cancer Med, 2024, 13(22): e70383.
5. 白娟, 蒲萍, 郑玲. 小细胞肺癌发生骨转移及骨相关事件的风险因素分析. 现代肿瘤医学, 2019, 27(16): 2876-2879.Bai J, Pu P, Zheng L. Risk factors of bone metastasis and bone-related events in small cell lung cancer. Modern Oncol, 2019, 27(16): 2876-2879.
6. Gao Y, Wu M, Rizvi SAA, et al. Exploring the key pathogenic mechanisms and potential intervention targets for Sophorae Flavescentis radix in managing bone metastasis of lung cancer based on network pharmacology and molecular docking techniques. Transl Cancer Res, 2024, 13(10): 5616-5626.
7. Wu B, Zhu Y, Hu Z, et al. Machine learning predictive models and risk factors for lymph node metastasis in non-small cell lung cancer. BMC Pulm Med, 2024, 24(1): 526.
8. Asano Y, Yamamoto N, Hayashi K, et al. Serum inflammatory dynamics as novel biomarkers for immune checkpoint inhibitors in non-small-cell lung cancer with bone metastases. Anticancer Res, 2024, 44(10): 4493-4503.
9. Pu D, Zhang HE, Li L. Immune-related osteoblastic bone alterations mimicking bone metastasis in a small-cell lung cancer patient treated with durvalumab: a case report. Transl Lung Cancer Res, 2024, 13(8): 2043-2049.
10. Guo Y, Lin Q, Zhao S, et al. Automated detection of lung cancer-caused metastasis by classifying scintigraphic images using convolutional neural network with residual connection and hybrid attention mechanism. Insights Imaging, 2022, 13(1): 24.
11. Lin Z, Wang R, Zhou Y, et al. Prediction of distant metastasis and survival prediction of gastric cancer patients with metastasis to the liver, lung, bone, and brain: research based on the SEER database. Ann Transl Med, 2022, 10(1): 16.
12. Xiaoqing H, Luopeng B, Yunyun W, et al. Genetically engineered exosomes for targetedly preventing premetastatic niche formation and suppressing postoperative melanoma lung metastasis. Nano Today, 2022, 3(1): 46.
13. Akshaya RL, Saranya I, Salomi GM, et al. In vivo validation of the functional role of MicroRNA-4638-3p in breast cancer bone metastasis. J Cancer Res Clin Oncol, 2024, 150(2): 63.
14. Li T, Lin Q, Guo Y, et al. Automated detection of skeletal metastasis of lung cancer with bone scans using convolutional nuclear network. Phys Med Biol, 2022, 67(1): 014001.
15. Shi S, Wang H, Liu X, et al. Prediction of overall survival of non-small cell lung cancer with bone metastasis: an analysis of the Surveillance, Epidemiology and End Results (SEER) database. Transl Cancer Res, 2021, 10(12): 5191-5203.
16. Hong Q, Hu H, Liu D, et al. Bioinformatic analysis of differentially expressed genes in lung cancer bone metastasis and their implications for disease progression in lung cancer patients. J Thorac Dis, 2024, 16(7): 4666-4677.
17. Guo J, Miao J, Sun W, et al. Predicting bone metastasis-free survival in non-small cell lung cancer from preoperative CT via deep learning. NPJ Precis Oncol, 2024, 8(1): 161.
18. Badhe PV, Sivakumar M, Lamture S, et al. White out hemithorax secondary to salivary gland type of lung cancer with metastasis in liver and bone: a case report. J Med Case Rep, 2024, 18(1): 288.
19. Zhong N, Wang H, Zhao W, et al. High RNF7 expression enhances PD-1 resistance of non-small cell lung cancer cells by promoting CXCL1 expression and myeloid-derived suppressor cell recruitment via activating NF-κB signaling. Nan Fang Yi Ke Da Xue Xue Bao, 2024, 44(9): 1704-1711. Zhong N, Wang H, Zhao W, et al. High RNF7 expression enhances PD-1 resistance of non-small cell lung cancer cells by promoting CXCL1 expression and myeloid-derived suppressor cell recruitment via activating NF-κB signaling. J South Med Univ, 2024, 44(9): 1704-1711.
20. Han L, Huang Z, Liu Y, et al. MicroRNA-106a regulates autophagy-related cell death and EMT by targeting TP53INP1 in lung cancer with bone metastasis. Cell Death Dis, 2021, 12(11): 1037.
21. Lu Y, Ma J, Li Y, et al. Correction: CDP138 silencing inhibits TGF-β/Smad signaling to impair radioresistance and metastasis via GDF15 in lung cancer. Cell Death Dis, 2024, 15(7): 549.
22. Liu G, Zhang H. ANGPT1 promotes M1 macrophage polarization and inhibits lung adenocarcinoma progression by inhibiting the TGF-β signalling pathway. Gen Physiol Biophys, 2024, 43(2): 121-138.
23. 金依诺, 汤心雨, 刘雯雯, 等. 靶向肿瘤微环境的肺癌脑转移研究进展. 中华医学杂志, 2024, 104(18): 1641-1648.Jin YN, Tang XY, Liu WW, et al. Research progress on brain metastasis of lung cancer targeting tumor microenvironment. Natl Med J China, 2024, 104(18): 1641-1648.
24. Chen P, Min J, Wu H, et al. Annexin A1 is a potential biomarker of bone metastasis in small cell lung cancer. Oncol Lett, 2021, 21(2): 141.
25. Liu Q, Dong Y, Ren S, et al. GPNMB associates with inferior prognosis in SCLC patients through promoting tumor cell metastasis. J Thorac Oncol, 2021, 16(10): 1194-1195.
26. Zhang H, Zhao B, Zhai ZG, et al. Expression and clinical significance of MMP-9 and P53 in lung cancer. Eur Rev Med Pharmacol Sci, 2021, 25(3): 1358-1365.
27. Zhang C, Zhou Y, Zhang B, et al. Identification of lncRNA, miRNA and mRNA expression profiles and ceRNA networks in small cell lung cancer. BMC Genomics, 2023, 24(1): 217.
28. 洪克林, 黄进启, 郑勇, 等. 血清CaN、COX2、TK1、Ca2+及ALP联合检测用于肺癌骨转移诊断的价值. 国际检验医学杂志, 2021, 42(4): 504-508.Hong KL, Huang JQ, Zheng Y, et al. The value of combined detection of serum CaN, COX2, TK1, Ca2+ and ALP in the diagnosis of bone metastasis of lung cancer. Int J Lab Med, 2021, 42(4): 504-508.
29. 张双捷, 王立峰. 血清ALP、PINP、PTHrP对肺癌骨转移诊断的价值. 东南大学学报(医学版), 2020, 39(3): 309-314.Zhang SJ, Wang LF. Diagnostic value of serum ALP, PINP and PTHrP for bone metastasis of lung cancer. J Southeast Univ Med Sci Ed, 2020, 39(3): 309-314.
30. 林敏, 朱柳君, 莫春香, 等. 骨代谢标志物在前列腺癌骨转移患者血清中的表达水平及其诊断价值. 广西医学, 2021, 43(9): 1074-1077.Lin M, Zhu LJ, Mo CX, et al. Expression level of bone metabolic markers in serum of patients with bone metastasis of prostate cancer and its diagnostic value. Guangxi Med J, 2021, 43(9): 1074-1077.
31. 康翠伟, 闫利鹏, 刘宁, 等. 溶骨性骨代谢标志物血Ⅰ型CTP、miR-107及TRACP-5b检测在肺癌骨转移中的诊断价值. 分子诊断与治疗杂志, 2024, 16(2): 331-334.Kang CW, Yan LP, Liu N, et al. Diagnostic value of serum type Ⅰ CTP, miR-107 and TRACP-5b as markers of osteolytic bone metabolism in bone metastasis of lung cancer. J Mol Diagn Ther, 2024, 16(2): 331-334.
32. Congedo MT, Nachira D, Bertolaccini L, et al. Multimodal therapy for synchronous bone oligometastatic NSCLC: The role of surgery. J Surg Oncol, 2022, 125(4): 782-789.
33. Zhu S, Ge T, Hu J, et al. Prognostic value of surgical intervention in advanced lung adenocarcinoma: a population-based study. J Thorac Dis, 2021, 13(10): 5942-5953.
34. Sun Z, Sui X, Yang F, et al. Effects of primary tumor resection on the survival of patients with stage IV extrathoracic metastatic non-small cell lung cancer: a population-based study. Lung Cancer, 2019, 129: 98-106.
35. 郭连洪, 赵素花, 李斌, 等. 大剂量和常规分割剂量调强适形放疗联合89SrCl2静脉注射治疗肺癌骨转移的效果. 中国医学物理学杂志, 2020, 37(9): 1111-1114.Guo LH, Zhao SH, Li B, et al. Effect of high-dose and conventional fractionated dose intensity modulated radiotherapy combined with intravenous injection of 89SrCl2 on bone metastasis of lung cancer. Chin J Med Phys, 2020, 37(9): 1111-1114.
36. 徐阳, 李红云, 苏丹, 等. 伊班膦酸钠联合化疗对非小细胞肺癌骨转移患者炎性因子及骨代谢指标的影响. 实用临床医药杂志, 2022, 26(2): 52-55.Xu Y, Li HY, Su D, et al. Effects of ibandronate combined with chemotherapy on inflammatory factors and bone metabolism indexes in patients with bone metastasis from non-small cell lung cancer. J Clin Med Pract, 2022, 26(2): 52-55.
37. Meng C, Ge X, Tian J, et al. Prognostic role of targeted therapy in patients with multiple-site metastases from non-small-cell lung cancer. Future Oncol, 2020, 16(26): 1957-1967.
38. 周艳, 邵丽丽, 王晓丽, 等. 地舒单抗联合免疫检查点抑制剂治疗实体瘤骨转移临床疗效及安全性. 现代生物医学进展, 2023, 23(13): 2563-2567,2590.Zhou Y, Shao LL, Wang XL, et al. Clinical efficacy and safety of denosumab combined with immune checkpoint inhibitor in the treatment of bone metastasis of solid tumor. Prog Mod Biomed, 2023, 23(13): 2563-2567,2590.
39. 段登科, 白智龙, 温振涛, 等. 地舒单抗治疗非小细胞肺癌骨转移临床疗效. 临床军医杂志, 2024, 52(4): 410-412.Duan DK, Bai ZL, Wen ZT, et al. Clinical effect of denosumab on bone metastasis of non-small cell lung cancer. J Clin Mil Med, 2024, 52(4): 410-412.
40. 宋飞, 向盈盈, 张纪贵, 等. 经桡动脉途径与股动脉途径介入治疗肺鳞癌的对比. 昆明医科大学学报, 2021, 42(9): 134-137.Song F, Xiang YY, Zhang JG, et al. Comparison of interventional therapy for lung squamous cell carcinoma via radial artery and femoral artery. J Kunming Med Univ, 2021, 42(9): 134-137.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Latest ArticlesResearch progress and prospect of molecular mechanism, biomarkers and treatment of bone metastasis in lung cancer

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