The significance of sarcomatoid and rhabdoid dedifferentiation in renal cell carcinoma

Siegel, 2022, Cancer statistics, CA Cancer J. Clin., 72, 7, 10.3322/caac.21708 Lopez-Beltran, 2006, 2004 WHO classification of the renal tumors of the adults, Eur. Urol., 49, 798, 10.1016/j.eururo.2005.11.035 Delahunt, 2013, The International Society of Urological Pathology (ISUP) grading system for renal cell carcinoma and other prognostic parameters, Am. J. Surg. Pathol., 37, 1490, 10.1097/PAS.0b013e318299f0fb Fuhrman, 1982, Prognostic significance of morphologic parameters in renal cell carcinoma, Am. J. Surg. Pathol., 6, 655, 10.1097/00000478-198210000-00007 Skinner, 1971, Diagnosis and management of renal cell carcinoma. A clinical and pathologic study of 309 cases, Cancer, 28, 1165, 10.1002/1097-0142(1971)28:5<1165::AID-CNCR2820280513>3.0.CO;2-G Cheville, 2004, Sarcomatoid renal cell carcinoma: an examination of underlying histologic subtype and an analysis of associations with patient outcome, Am. J. Surg. Pathol., 28, 435, 10.1097/00000478-200404000-00002 Shuch, 2010, Histologic evaluation of metastases in renal cell carcinoma with sarcomatoid transformation and its implications for systemic therapy, Cancer, 116, 616, 10.1002/cncr.24768 Reuter, 1993, Sarcomatoid lesions of the urogenital tract, Semin. Diagn. Pathol., 10, 188 Ozcan, 2012, PAX2 and PAX8 expression in primary and metastatic renal tumors: a comprehensive comparison, Arch. Pathol. Lab. Med., 136, 1541, 10.5858/arpa.2012-0072-OA Blum, 2020, Sarcomatoid renal cell carcinoma: biology, natural history and management, Nat. Rev. Urol., 17, 659, 10.1038/s41585-020-00382-9 Gökden, 2000, Renal cell carcinoma with rhabdoid features, Am. J. Surg. Pathol., 24, 1329, 10.1097/00000478-200010000-00002 Kuroiwa, 2002, Renal cell carcinoma with rhabdoid features: an aggressive neoplasm, Histopathology, 41, 538, 10.1046/j.1365-2559.2002.01427.x Leroy, 2007, Renal cell carcinoma with rhabdoid features: an aggressive neoplasm with overexpression of p53, Arch. Pathol. Lab. Med., 131, 102, 10.5858/2007-131-102-RCCWRF Shannon, 2002, Adult rhabdoid renal cell carcinoma, Arch. Pathol. Lab. Med., 126, 1506, 10.5858/2002-126-1506-ARRCC Shannon, 2003, Rhabdoid differentiation of chromophobe renal cell carcinoma, Pathology, 35, 228, 10.1080/0031302031000123209 Hahn, 2021, First-line immuno-oncology combinations for metastatic clear cell renal cell carcinoma (mRCC): a systematic review of phase III clinical trials, Kidney Cancer, 5, 207, 10.3233/KCA-210123 de Peralta-Venturina, 2001, Sarcomatoid differentiation in renal cell carcinoma: a study of 101 cases, Am. J. Surg. Pathol., 25, 275, 10.1097/00000478-200103000-00001 Mian, 2002, Prognostic factors and survival of patients with sarcomatoid renal cell carcinoma, J. Urol., 167, 65, 10.1016/S0022-5347(05)65384-0 Alevizakos, 2019, Sarcomatoid renal cell carcinoma: population-based study of 879 patients, Clin. Genitourin. Cancer, 17, 10.1016/j.clgc.2019.01.005 Trudeau, 2016, Comparison of oncologic outcomes between sarcomatoid and clear cell renal cell carcinoma, World J. Urol., 34, 1429, 10.1007/s00345-016-1780-z Zhang, 2015, A novel prognostic model for patients with sarcomatoid renal cell carcinoma, BJU Int., 115, 405, 10.1111/bju.12781 Adibi, 2015, Percentage of sarcomatoid component as a prognostic indicator for survival in renal cell carcinoma with sarcomatoid dedifferentiation, Urol. Oncol., 33, 10.1016/j.urolonc.2015.04.011 Kim, 2015, Using percentage of sarcomatoid differentiation as a prognostic factor in renal cell carcinoma, Clin. Genitourin. Cancer, 13, 225, 10.1016/j.clgc.2014.12.001 Shuch, 2012, Impact of pathological tumour characteristics in patients with sarcomatoid renal cell carcinoma, BJU Int., 109, 1600, 10.1111/j.1464-410X.2011.10785.x Casuscelli, 2019, Chromophobe renal cell carcinoma: results from a large single-institution series, Clin. Genitourin. Cancer, 17, 10.1016/j.clgc.2019.06.011 Pieretti, 2021, Sarcomatoid features and lymph node-positive disease in chromophobe renal cell carcinoma, Urol. Oncol., 39, 10.1016/j.urolonc.2021.06.016 Whaley, 2022, Clinicopathologic and immunohistochemical characterization of sarcomatoid chromophobe renal cell carcinoma: an analysis of 22 cases, Am. J. Surg. Pathol., 10.1097/PAS.0000000000001926 Zoumpourlis, 2021, Systemic therapies for the management of non-clear cell renal cell carcinoma: what works, what doesn't, and what the future holds, Clin. Genitourin. Cancer, 19, 103, 10.1016/j.clgc.2020.11.005 Merrill, 2015, Clinically nonmetastatic renal cell carcinoma with sarcomatoid dedifferentiation: natural history and outcomes after surgical resection with curative intent, Urol. Oncol., 33, 10.1016/j.urolonc.2014.11.021 Dudani, 2021, Evaluation of clear cell, papillary, and chromophobe renal cell carcinoma metastasis sites and association with survival, JAMA Netw. Open, 4, 10.1001/jamanetworkopen.2020.21869 Zhang, 2015, Impact of rhabdoid differentiation on prognosis for patients with grade 4 renal cell carcinoma, Eur. Urol., 68, 5, 10.1016/j.eururo.2015.01.002 Kara, 2016, Prognostic implications of sarcomatoid and rhabdoid differentiation in patients with grade 4 renal cell carcinoma, Int. Urol. Nephrol., 48, 1253, 10.1007/s11255-016-1314-z Delahunt, 1999, Sarcomatoid renal carcinoma: the final common dedifferentiation pathway of renal epithelial malignancies, Pathology, 31, 185, 10.1080/003130299104945 Conant, 2011, Sarcomatoid renal cell carcinoma is an example of epithelial–mesenchymal transition, J. Clin. Pathol., 64, 1088, 10.1136/jclinpath-2011-200216 Jones, 2005, Clonal divergence and genetic heterogeneity in clear cell renal cell carcinomas with sarcomatoid transformation, Cancer, 104, 1195, 10.1002/cncr.21288 Tickoo, 2007, Immunohistochemical expression of hypoxia inducible factor-1alpha and its downstream molecules in sarcomatoid renal cell carcinoma, J. Urol., 177, 1258, 10.1016/j.juro.2006.11.100 Bi, 2016, Genomic characterization of sarcomatoid transformation in clear cell renal cell carcinoma, Proc. Natl. Acad. Sci. U. S. A., 113, 2170, 10.1073/pnas.1525735113 Ramesh, 2020, Targeting EMT in cancer with repurposed metabolic inhibitors, Trends Cancer, 6, 942, 10.1016/j.trecan.2020.06.005 Malouf, 2016, Genomic characterization of renal cell carcinoma with sarcomatoid dedifferentiation pinpoints recurrent genomic alterations, Eur. Urol., 70, 348, 10.1016/j.eururo.2016.01.051 Wang, 2017, Sarcomatoid renal cell carcinoma has a distinct molecular pathogenesis, driver mutation profile, and transcriptional landscape, Clin. Cancer Res., 23, 6686, 10.1158/1078-0432.CCR-17-1057 Malouf, 2020, Molecular characterization of sarcomatoid clear cell renal cell carcinoma unveils new candidate oncogenic drivers, Sci. Rep., 10, 10.1038/s41598-020-57534-5 Motzer, 2020, Molecular subsets in renal cancer determine outcome to checkpoint and angiogenesis blockade, Cancer Cell, 38, 10.1016/j.ccell.2020.10.011 Agaimy, 2017, Rhabdoid and undifferentiated phenotype in renal cell carcinoma: analysis of 32 cases indicating a distinctive common pathway of dedifferentiation frequently associated with SWI/SNF complex deficiency, Am. J. Surg. Pathol., 41, 253, 10.1097/PAS.0000000000000787 Pawel, 2018, SMARCB1-deficient tumors of childhood: a practical guide, Pediatr. Dev. Pathol., 21, 6, 10.1177/1093526617749671 Singh, 2015, Intratumoral morphologic and molecular heterogeneity of rhabdoid renal cell carcinoma: challenges for personalized therapy, Mod. Pathol., 28, 1225, 10.1038/modpathol.2015.68 Bakouny, 2021, Integrative molecular characterization of sarcomatoid and rhabdoid renal cell carcinoma, Nat. Commun., 12, 10.1038/s41467-021-21068-9 Tannir, 2021, Efficacy and safety of nivolumab plus ipilimumab versus sunitinib in first-line treatment of patients with advanced sarcomatoid renal cell carcinoma, Clin. Cancer Res., 27, 78, 10.1158/1078-0432.CCR-20-2063 Sella, 1987, Sarcomatoid renal cell carcinoma. A treatable entity, Cancer, 60, 1313, 10.1002/1097-0142(19870915)60:6<1313::AID-CNCR2820600625>3.0.CO;2-1 Culine, 1995, Treatment of sarcomatoid renal cell carcinoma: is there a role for chemotherapy?, Eur. Urol., 27, 138, 10.1159/000475145 Escudier, 2002, Doxorubicin and ifosfamide in patients with metastatic sarcomatoid renal cell carcinoma: a phase II study of the Genitourinary Group of the French Federation of Cancer Centers, J. Urol., 168, 959, 10.1016/S0022-5347(05)64551-X Nanus, 2004, Active chemotherapy for sarcomatoid and rapidly progressing renal cell carcinoma, Cancer, 101, 1545, 10.1002/cncr.20541 Haas, 2012, A phase II trial of doxorubicin and gemcitabine in renal cell carcinoma with sarcomatoid features: ECOG 8802, Med. Oncol., 29, 761, 10.1007/s12032-011-9829-8 Motzer, 2022, Kidney cancer, version 3.2022, NCCN clinical practice guidelines in oncology, J. Natl. Compr. Canc. Netw., 20, 71, 10.6004/jnccn.2022.0001 Golshayan, 2009, Metastatic sarcomatoid renal cell carcinoma treated with vascular endothelial growth factor-targeted therapy, J. Clin. Oncol., 27, 235, 10.1200/JCO.2008.18.0000 Kyriakopoulos, 2015, Outcome of patients with metastatic sarcomatoid renal cell carcinoma: results from the International Metastatic Renal Cell Carcinoma Database Consortium, Clin. Genitourin. Cancer, 13, e79, 10.1016/j.clgc.2014.08.011 Keskin, 2017, Outcomes of patients with renal cell carcinoma and sarcomatoid dedifferentiation treated with nephrectomy and systemic therapies: comparison between the cytokine and targeted therapy eras, J. Urol., 198, 530, 10.1016/j.juro.2017.04.067 Staehler, 2010, Sorafenib after combination therapy with gemcitabine plus doxorubicine in patients with sarcomatoid renal cell carcinoma: a prospective evaluation, Eur. J. Med. Res., 15, 287, 10.1186/2047-783X-15-7-287 Michaelson, 2015, Phase 2 trial of sunitinib and gemcitabine in patients with sarcomatoid and/or poor-risk metastatic renal cell carcinoma, Cancer, 121, 3435, 10.1002/cncr.29503 Maiti, 2017, Phase 2 trial of capecitabine, gemcitabine, and bevacizumab in sarcomatoid renal-cell carcinoma, Clin. Genitourin. Cancer Haas, 2016, ECOG 1808: randomized phase II trial of sunitinib with or without gemcitabine in advanced kidney cancer with sarcomatoid features, J. Clin. Oncol., 34, 4511, 10.1200/JCO.2016.34.15_suppl.4511 Park, 2019, A multicenter, prospective phase II trial of gemcitabine plus axitinib in patients with renal cell carcinoma with a predominant sarcomatoid component, Invest. New Drugs, 37, 1239, 10.1007/s10637-019-00817-0 Santoni, 2021, Cabozantinib in pretreated patients with metastatic renal cell carcinoma with sarcomatoid differentiation: a real-world study, Target Oncol., 16, 625, 10.1007/s11523-021-00828-z Sharma, 2021, The next decade of immune checkpoint therapy, Cancer Discov., 11, 838, 10.1158/2159-8290.CD-20-1680 Adashek, 2020, Recent advancements in the treatment of metastatic clear cell renal cell carcinoma: a review of the evidence using second-generation p-values, Cancer Treat. Res. Commun., 23 Tannir, 2022, Efficacy and safety of nivolumab plus ipilimumab (N+I) versus sunitinib (S) for first-line treatment of patients with advanced sarcomatoid renal cell carcinoma (sRCC) in the phase 3 CheckMate 214 trial with extended 5-year minimum follow-up, J. Clin. Oncol., 40, 352, 10.1200/JCO.2022.40.6_suppl.352 Rini, 2019, Pembrolizumab (pembro) plus axitinib (axi) versus sunitinib as first-line therapy for metastatic renal cell carcinoma (mRCC): outcomes in the combined IMDC intermediate/poor risk and sarcomatoid subgroups of the phase 3 KEYNOTE-426 study, J. Clin. Oncol., 37, 4500, 10.1200/JCO.2019.37.15_suppl.4500 Choueiri, 2021, Efficacy and correlative analyses of avelumab plus axitinib versus sunitinib in sarcomatoid renal cell carcinoma: post hoc analysis of a randomized clinical trial, ESMO Open, 6 Motzer, 2021, Nivolumab + cabozantinib (NIVO+CABO) versus sunitinib (SUN) for advanced renal cell carcinoma (aRCC): outcomes by sarcomatoid histology and updated trial results with extended follow-up of CheckMate 9ER, J. Clin. Oncol., 39, 308, 10.1200/JCO.2021.39.6_suppl.308 Choueiri, 2021, Phase III clear trial in advanced renal cell carcinoma (aRCC): outcomes in subgroups and toxicity update, Ann. Oncol., 32, 10.1016/j.annonc.2021.08.056 Rini, 2021, Atezolizumab plus bevacizumab versus sunitinib for patients with untreated metastatic renal cell carcinoma and sarcomatoid features: a prespecified subgroup analysis of the immotion151 clinical trial, Eur. Urol., 79, 659, 10.1016/j.eururo.2020.06.021 Chahoud, 2020, Nivolumab for the treatment of patients with metastatic non-clear cell renal cell carcinoma (nccRCC): a single-institutional experience and literature meta-analysis, Oncologist, 25, 252, 10.1634/theoncologist.2019-0372 Joseph, 2015, PD-1 and PD-L1 expression in renal cell carcinoma with sarcomatoid differentiation, Cancer Immunol. Res., 3, 1303, 10.1158/2326-6066.CIR-15-0150 Kawakami, 2017, Programmed cell death ligand 1 and tumor-infiltrating lymphocyte status in patients with renal cell carcinoma and sarcomatoid dedifferentiation, Cancer, 123, 4823, 10.1002/cncr.30937 Gupta, 2019, JAK2/PD-L1/PD-L2 (9p24.1) amplifications in renal cell carcinomas with sarcomatoid transformation: implications for clinical management, Mod. Pathol., 32, 1344, 10.1038/s41379-019-0269-x Schvartsman, 2019, Rapid deep responses with nivolumab plus ipilimumab in papillary renal cell carcinoma with sarcomatoid dedifferentiation, Clin. Genitourin. Cancer, 17, 315, 10.1016/j.clgc.2019.05.023 Choueiri, 2021, Adjuvant pembrolizumab after nephrectomy in renal-cell carcinoma, N. Engl. J. Med., 385, 683, 10.1056/NEJMoa2106391 Apolo, 2022, Evolving role of adjuvant systemic therapy for kidney and urothelial cancers, Am. Soc. Clin. Oncol. Educ. Book, 42, 1 Msaouel, 2021, Making patient-specific treatment decisions using prognostic variables and utilities of clinical outcomes, Cancers (Basel), 13, 10.3390/cancers13112741 Correa, 2021, Predicting disease recurrence, early progression, and overall survival following surgical resection for high-risk localized and locally advanced renal cell carcinoma, Eur. Urol., 80, 20, 10.1016/j.eururo.2021.02.025 Hahn, 2022, Missing the trees for the forest: most subgroup analyses using forest plots at the ASCO annual meeting are inconclusive, Ther. Adv. Med. Oncol., 14, 10.1177/17588359221103199