Response rate specific to bone metastasis of various cancers for immune checkpoint inhibitors: a systematic review.
Bone
Immune checkpoint inhibitors
Metastasis
Response
Specific
Journal
European journal of orthopaedic surgery & traumatology : orthopedie traumatologie
ISSN: 1432-1068
Titre abrégé: Eur J Orthop Surg Traumatol
Pays: France
ID NLM: 9518037
Informations de publication
Date de publication:
05 Jun 2024
05 Jun 2024
Historique:
received:
31
03
2024
accepted:
31
05
2024
medline:
5
6
2024
pubmed:
5
6
2024
entrez:
5
6
2024
Statut:
aheadofprint
Résumé
Immune checkpoint inhibitors (ICIs) have improved the prognosis of patients with cancer, such as melanoma, renal cell carcinoma, head and neck cancer, non-small cell lung cancer (NSCLC), and urothelial carcinoma. The extension of life expectancy has led to an increased incidence of bone metastases (BM) among patients with cancer. BM result in skeletal-related events, including severe pain, pathological fractures, and nerve palsy. Surgery is typically required for the treatment of BM in patients with an impending fracture; however, it may be avoided in those who respond to ICIs. We systematically reviewed studies analyzing BM responses to treatment with ICIs. This study was conducted in accordance with the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-analyses 2020 statement and registered in the UMIN Clinical Trials Registry (ID: UMIN000053707). Studies reporting response rates based on the Response Evaluation Criteria in Solid Tumors (RECIST) or the MD Anderson Cancer Center (MDA) criteria specific for BM in patients treated with ICIs were included; reports of fewer than five cases and review articles were excluded. Studies involving humans, published in English and Japanese, were searched. The PubMed, Embase, and the Cochrane Central Register of Controlled Trials (CENTRAL) databases were searched. Ultimately, nine studies were analyzed. The Risk of Bias Assessment tool for Non-randomized Studies was used to assess the quality of studies. Based on the MDA criteria, complete response (CR) or partial response (PR) was observed in 44-78% and 62% patients treated with ICIs plus denosumab for NSCLC and melanoma, respectively. According to the RECIST, CR or PR was recorded in 5% and 7-28% of patients treated with ICIs for renal cell carcinoma and urothelial carcinoma, respectively. Although response rates to ICIs for BM are poor, patients treated with ICI plus denosumab for bone metastases with impending fractures from NSCLC and melanoma are likely to avoid surgery to prevent fractures.
Identifiants
pubmed: 38836904
doi: 10.1007/s00590-024-04018-1
pii: 10.1007/s00590-024-04018-1
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag France SAS, part of Springer Nature.
Références
Haslam A, Prasad V (2019) Estimation of the percentage of US patients with cancer who are eligible for and respond to checkpoint inhibitor immunotherapy drugs. JAMA Netw Open 2:e192535. https://doi.org/10.1001/jamanetworkopen.2019.2535
doi: 10.1001/jamanetworkopen.2019.2535
pubmed: 31050774
pmcid: 6503493
Joseph GJ, Johnson DB, Johnson RW (2023) Immune checkpoint inhibitors in bone metastasis: clinical challenges, toxicities, and mechanisms. J Bone Oncol 43:100505. https://doi.org/10.1016/j.jbo.2023.100505
doi: 10.1016/j.jbo.2023.100505
pubmed: 37842554
pmcid: 10568292
Schmid S, Diem S, Li Q et al (2018) Organ-specific response to nivolumab in patients with non-small cell lung cancer (NSCLC). Cancer Immunol Immunother 67:1825–1832. https://doi.org/10.1007/s00262-018-2239-4
doi: 10.1007/s00262-018-2239-4
pubmed: 30171269
pmcid: 11028265
Qin A, Zhao S, Miah A et al (2021) Bone metastases, skeletal-related events, and survival in patients with metastatic non-small cell lung cancer treated with immune checkpoint inhibitors. J Natl Compr Canc Netw 19:915–921. https://doi.org/10.6004/jnccn.2020.7668
doi: 10.6004/jnccn.2020.7668
pubmed: 33878726
pmcid: 8752085
da Silva LM, da Silva GT, Bergmann A et al (2021) Impact of different patterns of metastasis in non-small-cell lung cancer patients. Future Oncol 17:775–782. https://doi.org/10.2217/fon-2020-0587
doi: 10.2217/fon-2020-0587
pubmed: 33508966
Landi L, D’Incà F, Gelibter A et al (2019) Bone metastases and immunotherapy in patients with advanced non-small-cell lung cancer. J Immunother Cancer 7:316. https://doi.org/10.1186/s40425-019-0793-8
doi: 10.1186/s40425-019-0793-8
pubmed: 31752994
pmcid: 6868703
Selvaggi G, Scagliotti GV (2005) Management of bone metastases in cancer: a review. Crit Rev Oncol Hematol 56:365–378. https://doi.org/10.1016/j.critrevonc.2005.03.011
doi: 10.1016/j.critrevonc.2005.03.011
pubmed: 15978828
Jiang W, Rixiati Y, Zhao B et al (2020) Incidence, prevalence, and outcomes of systemic malignancy with bone metastases. J Orthop Surg 28:2309499020915989. https://doi.org/10.1177/2309499020915989
doi: 10.1177/2309499020915989
Huang J-F, Shen J, Li X et al (2020) Incidence of patients with bone metastases at diagnosis of solid tumors in adults: a large population-based study. Ann Transl Med 8:482. https://doi.org/10.21037/atm.2020.03.55
doi: 10.21037/atm.2020.03.55
pubmed: 32395526
pmcid: 7210217
Woodward E, Jagdev S, McParland L et al (2011) Skeletal complications and survival in renal cancer patients with bone metastases. Bone 48:160–166. https://doi.org/10.1016/j.bone.2010.09.008
doi: 10.1016/j.bone.2010.09.008
pubmed: 20854942
Mavrogenis AF, Pala E, Romagnoli C et al (2012) Survival analysis of patients with femoral metastases. J Surg Oncol 105:135–141. https://doi.org/10.1002/jso.22061
doi: 10.1002/jso.22061
pubmed: 21815154
Asano Y, Yamamoto N, Demura S et al (2022) The therapeutic effect and clinical outcome of immune checkpoint inhibitors on bone metastasis in advanced non-small-cell lung cancer. Front Oncol 12:871675. https://doi.org/10.3389/fonc.2022.871675
doi: 10.3389/fonc.2022.871675
pubmed: 35433422
pmcid: 9010859
Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45:228–247. https://doi.org/10.1016/j.ejca.2008.10.026
doi: 10.1016/j.ejca.2008.10.026
pubmed: 19097774
Hamaoka T, Madewell JE, Podoloff DA et al (2004) Bone imaging in metastatic breast cancer. J Clin Oncol 22:2942–2953. https://doi.org/10.1200/JCO.2004.08.181
doi: 10.1200/JCO.2004.08.181
pubmed: 15254062
Mirels H (1989) Metastatic disease in long bones. A proposed scoring system for diagnosing impending pathologic fractures. Clin Orthop Relat Res 256–264
Del Conte A, De Carlo E, Bertoli E et al (2022) Bone metastasis and immune checkpoint inhibitors in non-small cell lung cancer (NSCLC): microenvironment and possible clinical implications. Int J Mol Sci 23:6832. https://doi.org/10.3390/ijms23126832
doi: 10.3390/ijms23126832
pubmed: 35743275
pmcid: 9224636
Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
doi: 10.1136/bmj.n71
pubmed: 33782057
pmcid: 8005924
Kim SY, Park JE, Lee YJ et al (2013) Testing a tool for assessing the risk of bias for nonrandomized studies showed moderate reliability and promising validity. J Clin Epidemiol 66:408–414. https://doi.org/10.1016/j.jclinepi.2012.09.016
doi: 10.1016/j.jclinepi.2012.09.016
pubmed: 23337781
Shimizu T, Miyake M, Nishimura N et al (2022) Organ-specific and mixed responses to pembrolizumab in patients with unresectable or metastatic urothelial carcinoma: a multicenter retrospective study. Cancers 14:1735. https://doi.org/10.3390/cancers14071735
doi: 10.3390/cancers14071735
pubmed: 35406508
pmcid: 8997142
De Giglio A, Deiana C, Di Federico A (2023) Bone-specific response according to MDA criteria predicts immunotherapy efficacy among advanced non-small cell lung cancer (NSCLC) patients. J Cancer Res Clin Oncol 149:1835–1847. https://doi.org/10.1007/s00432-022-04120-z
doi: 10.1007/s00432-022-04120-z
pubmed: 35750899
Asano Y, Yamamoto N, Demura S et al (2023) Novel predictors of immune checkpoint inhibitor response and prognosis in advanced non-small-cell lung cancer with bone metastasis. Cancer Med 12:12425–12437. https://doi.org/10.1002/cam4.5952
doi: 10.1002/cam4.5952
pubmed: 37076988
pmcid: 10278505
Bongiovanni A, Foca F, Menis J et al (2021) Immune checkpoint inhibitors with or without bone-targeted therapy in NSCLC patients with bone metastases and prognostic significance of neutrophil-to-lymphocyte ratio. Front Immunol 12:697298. https://doi.org/10.3389/fimmu.2021.697298
doi: 10.3389/fimmu.2021.697298
pubmed: 34858389
pmcid: 8631508
Negishi T, Furubayashi N, Nakagawa T et al (2021) Site-specific response to nivolumab in renal cell carcinoma. Anticancer Res 41:1539–1545. https://doi.org/10.21873/anticanres.14913
doi: 10.21873/anticanres.14913
pubmed: 33788747
Nakata E, Sugihara S, Sugawara Y et al (2020) Early response of bone metastases can predict tumor response in patients with non-small-cell lung cancer with bone metastases in the treatment with nivolumab. Oncol Lett 20:2977–2986. https://doi.org/10.3892/ol.2020.11856
doi: 10.3892/ol.2020.11856
pubmed: 32782615
pmcid: 7401004
Angela Y, Haferkamp S, Weishaupt C et al (2019) Combination of denosumab and immune checkpoint inhibition: experience in 29 patients with metastatic melanoma and bone metastases. Cancer Immunol Immunother 68:1187–1194. https://doi.org/10.1007/s00262-019-02353-5
doi: 10.1007/s00262-019-02353-5
pubmed: 31187176
pmcid: 11028174
Furubayashi N, Negishi T, Sakamoto N et al (2021) Organ-specific tumor response to pembrolizumab in advanced urothelial carcinoma after platinum-based chemotherapy. Onco Targets Ther 14:1981–1988. https://doi.org/10.2147/OTT.S299724
doi: 10.2147/OTT.S299724
pubmed: 33776447
pmcid: 7987306
Raparia K, Villa C, DeCamp MM et al (2013) Molecular profiling in non-small cell lung cancer: a step toward personalized medicine. Arch Pathol Lab Med 137:481–491. https://doi.org/10.5858/arpa.2012-0287-RA
doi: 10.5858/arpa.2012-0287-RA
pubmed: 23544937
Hoban KA, Downie S, Adamson DJA et al (2022) Mirels’ score for upper limb metastatic lesions: do we need a different cutoff for recommending prophylactic fixation? JSES Int 6:675–681. https://doi.org/10.1016/j.jseint.2022.03.006
doi: 10.1016/j.jseint.2022.03.006
pubmed: 35813136
pmcid: 9264023
Van der Linden YM, Dijkstra PDS, Kroon HM et al (2004) Comparative analysis of risk factors for pathological fracture with femoral metastases. J Bone Joint Surg Br 86:566–573
doi: 10.1302/0301-620X.86B4.14703
pubmed: 15174555
Goodheart JR, Cleary RJ, Damron TA, Mann KA (2015) Simulating activities of daily living with finite element analysis improves fracture prediction for patients with metastatic femoral lesions. J Orthop Res 33:1226–1234. https://doi.org/10.1002/jor.22887
doi: 10.1002/jor.22887
pubmed: 25761000
Damron TA, Nazarian A, Entezari V et al (2016) CT-based structural rigidity analysis is more accurate than mirels scoring for fracture prediction in metastatic femoral lesions. Clin Orthop Relat Res 474:643–651. https://doi.org/10.1007/s11999-015-4453-0
doi: 10.1007/s11999-015-4453-0
pubmed: 26169800
Sternheim A, Traub F, Trabelsi N et al (2020) When and where do patients with bone metastases actually break their femurs? Bone Joint J 102-B:638–645. https://doi.org/10.1302/0301-620X.102B5.BJJ-2019-1328.R2
doi: 10.1302/0301-620X.102B5.BJJ-2019-1328.R2
pubmed: 32349590
van der Wal CWPG, Eggermont F, Fiocco M et al (2020) Axial cortical involvement of metastatic lesions to identify impending femoral fractures; a clinical validation study. Radiother Oncol 144:59–64. https://doi.org/10.1016/j.radonc.2019.10.007
doi: 10.1016/j.radonc.2019.10.007
pubmed: 31733489
Bellamy EA, Nicholas D, Ward M et al (1987) Comparison of computed tomography and conventional radiology in the assessment of treatment response of lytic bony metastases in patients with carcinoma of the breast. Clin Radiol 38:351–355. https://doi.org/10.1016/s0009-9260(87)80207-6
doi: 10.1016/s0009-9260(87)80207-6
pubmed: 3621814
Ruggieri P, Mavrogenis AF, Casadei R et al (2010) Protocol of surgical treatment of long bone pathological fractures. Injury 41:1161–1167. https://doi.org/10.1016/j.injury.2010.09.018
doi: 10.1016/j.injury.2010.09.018
pubmed: 20947077
Wedin R, Bauer HCF (2005) Surgical treatment of skeletal metastatic lesions of the proximal femur: endoprosthesis or reconstruction nail? J Bone Joint Surg Br 87:1653–1657. https://doi.org/10.1302/0301-620X.87B12.16629
doi: 10.1302/0301-620X.87B12.16629
pubmed: 16326880
Fidler M (1981) Incidence of fracture through metastases in long bones. Acta Orthop Scand 52:623–627. https://doi.org/10.3109/17453678108992157
doi: 10.3109/17453678108992157
pubmed: 7331799
van der Linden YM, Kroon HM, Dijkstra SPDS et al (2003) Simple radiographic parameter predicts fracturing in metastatic femoral bone lesions: results from a randomised trial. Radiother Oncol 69:21–31. https://doi.org/10.1016/s0167-8140(03)00232-9
doi: 10.1016/s0167-8140(03)00232-9
pubmed: 14597353
Eggermont F, van der Wal G, Westhoff P et al (2020) Patient-specific finite element computer models improve fracture risk assessments in cancer patients with femoral bone metastases compared to clinical guidelines. Bone 130:115101. https://doi.org/10.1016/j.bone.2019.115101
doi: 10.1016/j.bone.2019.115101
pubmed: 31655223
Comito F, Ambrosini V, Sperandi F et al (2018) Osteoblastic bone response mimicking bone progression during treatment with pembrolizumab in advanced cutaneous melanoma. Anticancer Drugs 29:1026–1029. https://doi.org/10.1097/CAD.0000000000000689
doi: 10.1097/CAD.0000000000000689
pubmed: 30095443
Ito S, Tachimori Y, Terado Y et al (2021) Primary malignant melanoma of the esophagus successfully treated with nivolumab: a case report. J Med Case Rep 15:237. https://doi.org/10.1186/s13256-021-02821-6
doi: 10.1186/s13256-021-02821-6
pubmed: 33947459
pmcid: 8097988
Kageyama S-I, Yamaguchi S, Ito S et al (2016) A case report of using nivolumab for a malignant melanoma patient with rheumatoid arthritis. Int Cancer Conf J 5:192–196. https://doi.org/10.1007/s13691-016-0256-8
doi: 10.1007/s13691-016-0256-8
pubmed: 31149453
pmcid: 6498278
Lankes K, Hundorfean G, Harrer T et al (2016) Anti-TNF-refractory colitis after checkpoint inhibitor therapy: possible role of CMV-mediated immunopathogenesis. Oncoimmunology 5:e1128611. https://doi.org/10.1080/2162402X.2015.1128611
doi: 10.1080/2162402X.2015.1128611
pubmed: 27471608
pmcid: 4938313
Matull J, Livingstone E, Wetter A et al (2020) Durable Complete response in a melanoma patient with unknown primary, associated with sequential and severe multi-organ toxicity after a single dose of CTLA-4 plus PD-1 blockade: a case report. Front Oncol 10:592609. https://doi.org/10.3389/fonc.2020.592609
doi: 10.3389/fonc.2020.592609
pubmed: 33262949
pmcid: 7686558
Oliveira LJC, Gongora ABL, Barbosa FG et al (2018) Atypical response with bone pseudoprogression in a patient receiving nivolumab for advanced cutaneous squamous cell carcinoma. J Immunother Cancer 6:130. https://doi.org/10.1186/s40425-018-0444-5
doi: 10.1186/s40425-018-0444-5
pubmed: 30482243
pmcid: 6258146
Kokura K, Watanabe J, Takuma T et al (2023) A case of Avelumab response to multiple bone and lymph node metastases of plasmacytoid variant bladder cancer. Urol Case Rep 47:102358. https://doi.org/10.1016/j.eucr.2023.102358
doi: 10.1016/j.eucr.2023.102358
pubmed: 36852129
pmcid: 9958419
Laffi A, Cozzi G, Spada F et al (2022) Metachronous testicular metastases from merkel cell carcinoma (MCC): a case report and literature review. Am J Case Rep 23:e936552. https://doi.org/10.12659/AJCR.936552
doi: 10.12659/AJCR.936552
pubmed: 36031755
pmcid: 9438938
Tamada S, Ikarashi D, Tsuyukubo T et al (2022) Efficacy of combination therapy with pembrolizumab and axitinib for metastatic renal collecting duct cell carcinoma: a report on two cases. IJU Case Rep 5:438–441. https://doi.org/10.1002/iju5.12504
doi: 10.1002/iju5.12504
pubmed: 36341193
pmcid: 9626324
Yano M, Aso S, Sato M et al (2020) Pembrolizumab and radiotherapy for platinum-refractory recurrent uterine carcinosarcoma with an abscopal effect: a case report. Anticancer Res 40:4131–4135. https://doi.org/10.21873/anticanres.14412
doi: 10.21873/anticanres.14412
pubmed: 32620662
Gefard-Gontier E, Markich R, Zysman M et al (2022) Evolution of bone metastases in patients receiving at least three months of checkpoint inhibitors. Cancer Immunol Immunother 71:2609–2618. https://doi.org/10.1007/s00262-022-03180-x
doi: 10.1007/s00262-022-03180-x
pubmed: 35305123
pmcid: 10991876
Lind JSW, Postmus PE, Smit EF (2010) Osteoblastic bone lesions developing during treatment with erlotinib indicate major response in patients with non-small cell lung cancer: a brief report. J Thorac Oncol 5:554–557. https://doi.org/10.1097/JTO.0b013e3181d3e47e
doi: 10.1097/JTO.0b013e3181d3e47e
pubmed: 20357621
Coleman RE, Croucher PI, Padhani AR et al (2020) Bone metastases. Nat Rev Dis Primers 6:83. https://doi.org/10.1038/s41572-020-00216-3
doi: 10.1038/s41572-020-00216-3
pubmed: 33060614
Yamashita Y, Aoki T, Hanagiri T et al (2012) Osteosclerotic lesions in patients treated with gefitinib for lung adenocarcinomas: a sign of favorable therapeutic response. Skeletal Radiol 41:409–414. https://doi.org/10.1007/s00256-011-1253-9
doi: 10.1007/s00256-011-1253-9
pubmed: 21866322
Philipp TC, Mikula JD, Doung Y-C, Gundle KR (2020) Is there an association between prophylactic femur stabilization and survival in patients with metastatic bone disease? Clin Orthop Relat Res 478:540–546. https://doi.org/10.1097/CORR.0000000000000803
doi: 10.1097/CORR.0000000000000803
pubmed: 32168065
Ward WG, Holsenbeck S, Dorey FJ et al (2003) Metastatic disease of the femur: surgical treatment. Clin Orthop Relat Res. https://doi.org/10.1097/01.blo.0000093849.72468.82
doi: 10.1097/01.blo.0000093849.72468.82
pubmed: 14646728
McLynn RP, Ondeck NT, Grauer JN, Lindskog DM (2018) What is the adverse event profile after prophylactic treatment of femoral shaft or distal femur metastases? Clin Orthop Relat Res 476:2381–2388. https://doi.org/10.1097/CORR.0000000000000489
doi: 10.1097/CORR.0000000000000489
pubmed: 30260860
pmcid: 6259894
Aneja A, Jiang JJ, Cohen-Rosenblum A et al (2017) Thromboembolic disease in patients with metastatic femoral lesions: a comparison between prophylactic fixation and fracture fixation. J Bone Joint Surg Am 99:315–323. https://doi.org/10.2106/JBJS.16.00023
doi: 10.2106/JBJS.16.00023
pubmed: 28196033
Liu L, Shi Z, Qiu X (2023) Impact of bone metastasis on the prognosis of non-small cell lung cancer patients treated with immune checkpoint inhibitors: a systematic review and meta-analysis. Clin Transl Oncol. https://doi.org/10.1007/s12094-023-03300-8
doi: 10.1007/s12094-023-03300-8
pubmed: 38123874
pmcid: 11108937
Tsukamoto S, Kido A, Tanaka Y et al (2021) Current overview of treatment for metastatic bone disease. Curr Oncol 28:3347–3372. https://doi.org/10.3390/curroncol28050290
doi: 10.3390/curroncol28050290
pubmed: 34590591
pmcid: 8482272