Pathologic Complete Response After Preoperative Ipilimumab and Nivolumab in an HLRCC Patient with Stage III RenalCell Carcinoma
Main Article Content
Keywords
HLRCC, Fumarate hydratase-deficient RCC
Abstract
Hereditary leiomyomatosis and renal cell carcinoma (HLRCC) is a rare, aggressive hereditary cancer syndrome caused by germline mutations in the fumarate hydratase (FH) gene. Affected patients typically present with renal cell carcinoma (RCC) at a young age and often experience rapidly progressive disease and poor outcomes. Mean survival is significantly shorter for stages III and IV than for stages I and II (15.8 vs 80.7 months), underscoring the need for more effective therapeutic strategies. Here, we report an HLRCC patient with stage III RCC who achieved a pathologic complete response following one cycle of dual immune checkpoint blockade with nivolumab and ipilimumab and remains disease-free 15 months later. This case extends findings from previous reports and suggests that dual checkpoint blockade may result in clinically meaningful activity in a subset of patients.
References
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7. Bardella C, El-Bahrawy M, Frizzell N, Adam J, Ternette N, Hatipoglu E, et al. Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status. J Pathol. 2011;225(1):4–11. https://doi.org/10.1002/path.2932
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11. Menko FH, Maher ER, Schmidt LS, Middelton LA, Aittomaki K, Tomlinson I, et al. Hereditary leiomyomatosis and renal cell cancer (HLRCC): Renal cancer risk, surveillance and treatment. Fam Cancer. 2014;13(4):637–44. https://doi.org/10.1007/s10689-014-9735-2
12. Schmidt LS, Linehan WM. Hereditary leiomyomatosis and renal cell carcinoma. Int J Nephrol Renovasc Dis. 2014;7:253–60. https://doi.org/10.2147/IJNRD.S42097
13. Toro JR, Nickerson ML, Wei MH, Warren MB, Glenn GM, Turner ML, et al. Mutations in the fumarate hydratase gene cause hereditary leiomyomatosis and renal cell cancer in families in North America. Am J Hum Genet. 2003;73(1):95–106. https://doi.org/10.1086/376435
14. Forde C, Lim DHK, Alwan Y, Burghel G, Butland L, Cleaver R, et al. Hereditary leiomyomatosis and renal cell cancer: Clinical, molecular, and screening features in a cohort of 185 affected individuals. Eur Urol Oncol. 2020;3(6):764–72. https://doi.org/10.1016/j.euo.2019.11.002
15. Scharnitz T, Nakamura M, Koeppe E, Henry ML, Lowe L, Else T, et al. The spectrum of clinical and genetic findings in hereditary leiomyomatosis and renal cell cancer (HLRCC) with relevance to patient outcomes: A retrospective study from a large academic tertiary referral center. Am J Cancer Res. 2023;13(1):236–44.
16. Moch H, Amin MB, Berney DM, Comperat EM, Gill AJ, Hartmann A, et al. The 2022 World Health Organization classification of tumours of the urinary system and male genital organs—Part A: Renal, penile, and testicular tumours. Eur Urol. 2022;82(5):458–68. https://doi.org/10.1016/j.eururo.2022.06.016
17. Patel VM, Handler MZ, Schwartz RA, Lambert WC. Hereditary leiomyomatosis and renal cell cancer syndrome: An update and review. J Am Acad Dermatol. 2017;77(1):149–58. https://doi.org/10.1016/j.jaad.2017.01.023
18. Merino MJ, Torres-Cabala C, Pinto P, Linehan WM. The morphologic spectrum of kidney tumors in hereditary leiomyomatosis and renal cell carcinoma (HLRCC) syndrome. Am J Surg Pathol. 2007;31(10):1578–85. https://doi.org/10.1097/PAS.0b013e31804375b8
19. Kapur P, Amin MB, Chen Y-B, Cheville J, Hes O, Rakheja D, et al. Recent updates in pathology of renal cell carcinoma: Société Internationale d'Urologie; 2022. Available from: https://www.siu-urology.org/themes/web/assets/files/2023/icud_webpage/2nd-wuof-siu-icud-kidney-cancer-final-october17-2022.pdf
20. Yamasaki T, Tran TA, Oz OK, Raj GV, Schwarz RE, Deberardinis RJ, et al. Exploring a glycolytic inhibitor for the treatment of an FH-deficient type-2 papillary RCC. Nat Rev Urol. 2011;8(3):165–71. https://doi.org/10.1038/nrurol.2010.234
21. Srinivasan R, Gurram S, Singer EA, Sidana A, Al Harthy M, Ball MW, et al. Bevacizumab and erlotinib in hereditary and sporadic papillary kidney cancer. N Engl J Med. 2025;392(23):2346–56. https://doi.org/10.1056/NEJMoa2200900
22. Choi Y, Keam B, Kim M, Yoon S, Kim D, Choi JG, et al. Bevacizumab plus erlotinib combination therapy for advanced hereditary leiomyomatosis and renal cell carcinoma-associated renal cell carcinoma: A multicenter retrospective analysis in Korean patients. Cancer Res Treat. 2019;51(4):1549–56. https://doi.org/10.4143/crt.2019.086
23. Alaghehbandan R, Stehlik J, Trpkov K, Magi-Galluzzi C, Condom Mundo E, Pane Foix M, et al. Programmed death-1 (PD-1) receptor/PD-1 ligand (PD-L1) expression in fumarate hydratase-deficient renal cell carcinoma. Ann Diagn Pathol. 2017;29:17–22. https://doi.org/10.1016/j.anndiagpath.2017.04.007
24. Yu Y, Shen Q, Xia M, Huang C, Li X, He S, et al. Fumarate hydratase-deficient renal cell carcinoma: High intratumoral and peritumoral CD4-positive T cell infiltration density and high PD-L1 expression. World J Urol. 2025;43(1):567. https://doi.org/10.1007/s00345-025-05941-6
25. Sun G, Zhang X, Liang J, Pan X, Zhu S, Liu Z, et al. Integrated molecular characterization of fumarate hydratase-deficient renal cell carcinoma. Clin Cancer Res. 2021;27(6):1734–43. https://doi.org/10.1158/1078-0432.CCR-20-3788
26. Iribe Y, Furuya M, Shibata Y, Yasui M, Funahashi M, Ota J, et al. Complete response of hereditary leiomyomatosis and renal cell cancer (HLRCC)-associated renal cell carcinoma to nivolumab and ipilimumab combination immunotherapy by: A case report. Fam Cancer. 2021;20(1):75–80. https://doi.org/10.1007/s10689-020-00195-0
27. Wang T, Huang Y, Huang X, Lv Z, Tian S, Ma X, et al. Complete response of hereditary leiomyomatosis and renal cell cancer (HLRCC)-associated renal cell carcinoma to pembrolizumab immunotherapy: A case report. Front Oncol. 2021;11:735077. https://doi.org/10.3389/fonc.2021.735077
28. Gao F, Gu D, Zhang H, Shi C, Du F, Zheng B, et al. Case report: Response to immunotherapy and association with the fh gene in hereditary leiomyomatosis and renal cell cancer-associated renal cell cancer. BMC Med Genomics. 2024;17(1):215. https://doi.org/10.1186/s12920-024-01957-w
29. Howells E, Wigston L, Mackie G, Tran B, Nott L. Advanced fumarate hydratase-deficient renal cell carcinoma responding to combination immune checkpoint inhibitors. Can J Urol. 2023;30(3):11558–61.
30. Muller M, Ferlicot S, Guillaud-Bataille M, Le Teuff G, Genestie C, Deveaux S, et al. Reassessing the clinical spectrum associated with hereditary leiomyomatosis and renal cell carcinoma syndrome in French FH mutation carriers. Clin Genet. 2017;92(6):606–15. https://doi.org/10.1111/cge.13014
31. Sanchez-Heras AB, Castillejo A, Garcia-Diaz JD, Robledo M, Teule A, Sanchez R, et al. Hereditary leiomyomatosis and renal cell cancer syndrome in Spain: Clinical and genetic characterization. Cancers (Basel). 2020;12(11):3277. https://doi.org/10.3390/cancers12113277
32. Park I, Shim YS, Go H, Hong BS, Lee JL. Long-term response of metastatic hereditary leiomyomatosis and renal cell carcinoma syndrome associated renal cell carcinoma to bevacizumab plus erlotinib after temsirolimus and axitinib treatment failures. BMC Urol. 2019;19(1):51. https://doi.org/10.1186/s12894-019-0484-2
33. Motzer RJ, Jonasch E, Agarwal N, Alva A, Bagshaw H, Baine M, et al. NCCN Guidelines(R) insights: Kidney cancer, Version 2.2024. J Natl Compr Canc Netw. 2024;22(1):4–16. https://doi.org/10.6004/jnccn.2024.0008
34. Bai J, Huang J, Ye Y, Lin J, Wen Y, Cai Z, et al. Clinicopathologic and prognosis of 30 patients with FH-deficient renal cell carcinoma: A single-center retrospective study. BMC Cancer. 2025;25(1):1152. https://doi.org/10.1186/s12885-025-14562-6
35. Motzer RJ, Tannir NM, McDermott DF, Aren Frontera O, Melichar B, Choueiri TK, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378(14):1277–90. https://doi.org/10.1056/NEJMoa1712126
36. Tannir NM, Albiges L, McDermott DF, Burotto M, Choueiri TK, Hammers HJ, et al. Nivolumab plus ipilimumab versus sunitinib for first-line treatment of advanced renal cell carcinoma: Extended 8-year follow-up results of efficacy and safety from the phase III CheckMate 214 trial. Ann Oncol. 2024;35(11):1026–38. https://doi.org/10.1016/j.annonc.2024.07.727
2. Stewart L, Glenn GM, Stratton P, Goldstein AM, Merino MJ, Tucker MA, et al. Association of germline mutations in the fumarate hydratase gene and uterine fibroids in women with hereditary leiomyomatosis and renal cell cancer. Arch Dermatol. 2008;144(12):1584–92. https://doi.org/10.1001/archdermatol.2008.517
3. Smit DL, Mensenkamp AR, Badeloe S, Breuning MH, Simon ME, van Spaendonck KY, et al. Hereditary leiomyomatosis and renal cell cancer in families referred for fumarate hydratase germline mutation analysis. Clin Genet. 2011;79(1):49–59. https://doi.org/10.1111/j.1399-0004.2010.01486.x
4. Gardie B, Remenieras A, Kattygnarath D, Bombled J, Lefevre S, Perrier-Trudova V, et al. Novel FH mutations in families with hereditary leiomyomatosis and renal cell cancer (HLRCC) and patients with isolated type 2 papillary renal cell carcinoma. J Med Genet. 2011;48(4):226–34. https://doi.org/10.1136/jmg.2010.085068
5. Alam NA, Bevan S, Churchman M, Barclay E, Barker K, Jaeger EE, et al. Localization of a gene (MCUL1) for multiple cutaneous leiomyomata and uterine fibroids to chromosome 1q42.3-q43. Am J Hum Genet. 2001;68(5):1264–9. https://doi.org/10.1086/320124
6. Kamihara J, Schultz KA, Rana HQ. FH tumor predisposition syndrome. In: Adam MP, Feldman J, Mirzaa GM, Pagon RA, Wallace SE, Amemiya A, editors. GeneReviews((R)). Seattle (WA): University of Washington, Seattle; 1993.
7. Bardella C, El-Bahrawy M, Frizzell N, Adam J, Ternette N, Hatipoglu E, et al. Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status. J Pathol. 2011;225(1):4–11. https://doi.org/10.1002/path.2932
8. Buelow B, Cohen J, Nagymanyoki Z, Frizzell N, Joseph NM, McCalmont T, et al. Immunohistochemistry for 2-succinocysteine (2SC) and fumarate hydratase (FH) in cutaneous leiomyomas may aid in identification of patients with HLRCC (hereditary leiomyomatosis and renal cell carcinoma syndrome). Am J Surg Pathol. 2016;40(7):982–8. https://doi.org/10.1097/PAS.0000000000000626
9. Kinch L, Grishin NV, Brugarolas J. Succination of Keap1 and activation of Nrf2-dependent antioxidant pathways in FH-deficient papillary renal cell carcinoma type 2. Cancer Cell. 2011;20(4):418–20. https://doi.org/10.1016/j.ccr.2011.10.005
10. Hamza A, Sirohi D, Smith SC, Amin MB. Low-grade oncocytic fumarate hydratase-deficient renal cell carcinoma: An update on biologic potential, morphologic spectrum, and differential diagnosis with other low-grade oncocytic tumors. Adv Anat Pathol. 2021;28(6):396–407. https://doi.org/10.1097/PAP.0000000000000321
11. Menko FH, Maher ER, Schmidt LS, Middelton LA, Aittomaki K, Tomlinson I, et al. Hereditary leiomyomatosis and renal cell cancer (HLRCC): Renal cancer risk, surveillance and treatment. Fam Cancer. 2014;13(4):637–44. https://doi.org/10.1007/s10689-014-9735-2
12. Schmidt LS, Linehan WM. Hereditary leiomyomatosis and renal cell carcinoma. Int J Nephrol Renovasc Dis. 2014;7:253–60. https://doi.org/10.2147/IJNRD.S42097
13. Toro JR, Nickerson ML, Wei MH, Warren MB, Glenn GM, Turner ML, et al. Mutations in the fumarate hydratase gene cause hereditary leiomyomatosis and renal cell cancer in families in North America. Am J Hum Genet. 2003;73(1):95–106. https://doi.org/10.1086/376435
14. Forde C, Lim DHK, Alwan Y, Burghel G, Butland L, Cleaver R, et al. Hereditary leiomyomatosis and renal cell cancer: Clinical, molecular, and screening features in a cohort of 185 affected individuals. Eur Urol Oncol. 2020;3(6):764–72. https://doi.org/10.1016/j.euo.2019.11.002
15. Scharnitz T, Nakamura M, Koeppe E, Henry ML, Lowe L, Else T, et al. The spectrum of clinical and genetic findings in hereditary leiomyomatosis and renal cell cancer (HLRCC) with relevance to patient outcomes: A retrospective study from a large academic tertiary referral center. Am J Cancer Res. 2023;13(1):236–44.
16. Moch H, Amin MB, Berney DM, Comperat EM, Gill AJ, Hartmann A, et al. The 2022 World Health Organization classification of tumours of the urinary system and male genital organs—Part A: Renal, penile, and testicular tumours. Eur Urol. 2022;82(5):458–68. https://doi.org/10.1016/j.eururo.2022.06.016
17. Patel VM, Handler MZ, Schwartz RA, Lambert WC. Hereditary leiomyomatosis and renal cell cancer syndrome: An update and review. J Am Acad Dermatol. 2017;77(1):149–58. https://doi.org/10.1016/j.jaad.2017.01.023
18. Merino MJ, Torres-Cabala C, Pinto P, Linehan WM. The morphologic spectrum of kidney tumors in hereditary leiomyomatosis and renal cell carcinoma (HLRCC) syndrome. Am J Surg Pathol. 2007;31(10):1578–85. https://doi.org/10.1097/PAS.0b013e31804375b8
19. Kapur P, Amin MB, Chen Y-B, Cheville J, Hes O, Rakheja D, et al. Recent updates in pathology of renal cell carcinoma: Société Internationale d'Urologie; 2022. Available from: https://www.siu-urology.org/themes/web/assets/files/2023/icud_webpage/2nd-wuof-siu-icud-kidney-cancer-final-october17-2022.pdf
20. Yamasaki T, Tran TA, Oz OK, Raj GV, Schwarz RE, Deberardinis RJ, et al. Exploring a glycolytic inhibitor for the treatment of an FH-deficient type-2 papillary RCC. Nat Rev Urol. 2011;8(3):165–71. https://doi.org/10.1038/nrurol.2010.234
21. Srinivasan R, Gurram S, Singer EA, Sidana A, Al Harthy M, Ball MW, et al. Bevacizumab and erlotinib in hereditary and sporadic papillary kidney cancer. N Engl J Med. 2025;392(23):2346–56. https://doi.org/10.1056/NEJMoa2200900
22. Choi Y, Keam B, Kim M, Yoon S, Kim D, Choi JG, et al. Bevacizumab plus erlotinib combination therapy for advanced hereditary leiomyomatosis and renal cell carcinoma-associated renal cell carcinoma: A multicenter retrospective analysis in Korean patients. Cancer Res Treat. 2019;51(4):1549–56. https://doi.org/10.4143/crt.2019.086
23. Alaghehbandan R, Stehlik J, Trpkov K, Magi-Galluzzi C, Condom Mundo E, Pane Foix M, et al. Programmed death-1 (PD-1) receptor/PD-1 ligand (PD-L1) expression in fumarate hydratase-deficient renal cell carcinoma. Ann Diagn Pathol. 2017;29:17–22. https://doi.org/10.1016/j.anndiagpath.2017.04.007
24. Yu Y, Shen Q, Xia M, Huang C, Li X, He S, et al. Fumarate hydratase-deficient renal cell carcinoma: High intratumoral and peritumoral CD4-positive T cell infiltration density and high PD-L1 expression. World J Urol. 2025;43(1):567. https://doi.org/10.1007/s00345-025-05941-6
25. Sun G, Zhang X, Liang J, Pan X, Zhu S, Liu Z, et al. Integrated molecular characterization of fumarate hydratase-deficient renal cell carcinoma. Clin Cancer Res. 2021;27(6):1734–43. https://doi.org/10.1158/1078-0432.CCR-20-3788
26. Iribe Y, Furuya M, Shibata Y, Yasui M, Funahashi M, Ota J, et al. Complete response of hereditary leiomyomatosis and renal cell cancer (HLRCC)-associated renal cell carcinoma to nivolumab and ipilimumab combination immunotherapy by: A case report. Fam Cancer. 2021;20(1):75–80. https://doi.org/10.1007/s10689-020-00195-0
27. Wang T, Huang Y, Huang X, Lv Z, Tian S, Ma X, et al. Complete response of hereditary leiomyomatosis and renal cell cancer (HLRCC)-associated renal cell carcinoma to pembrolizumab immunotherapy: A case report. Front Oncol. 2021;11:735077. https://doi.org/10.3389/fonc.2021.735077
28. Gao F, Gu D, Zhang H, Shi C, Du F, Zheng B, et al. Case report: Response to immunotherapy and association with the fh gene in hereditary leiomyomatosis and renal cell cancer-associated renal cell cancer. BMC Med Genomics. 2024;17(1):215. https://doi.org/10.1186/s12920-024-01957-w
29. Howells E, Wigston L, Mackie G, Tran B, Nott L. Advanced fumarate hydratase-deficient renal cell carcinoma responding to combination immune checkpoint inhibitors. Can J Urol. 2023;30(3):11558–61.
30. Muller M, Ferlicot S, Guillaud-Bataille M, Le Teuff G, Genestie C, Deveaux S, et al. Reassessing the clinical spectrum associated with hereditary leiomyomatosis and renal cell carcinoma syndrome in French FH mutation carriers. Clin Genet. 2017;92(6):606–15. https://doi.org/10.1111/cge.13014
31. Sanchez-Heras AB, Castillejo A, Garcia-Diaz JD, Robledo M, Teule A, Sanchez R, et al. Hereditary leiomyomatosis and renal cell cancer syndrome in Spain: Clinical and genetic characterization. Cancers (Basel). 2020;12(11):3277. https://doi.org/10.3390/cancers12113277
32. Park I, Shim YS, Go H, Hong BS, Lee JL. Long-term response of metastatic hereditary leiomyomatosis and renal cell carcinoma syndrome associated renal cell carcinoma to bevacizumab plus erlotinib after temsirolimus and axitinib treatment failures. BMC Urol. 2019;19(1):51. https://doi.org/10.1186/s12894-019-0484-2
33. Motzer RJ, Jonasch E, Agarwal N, Alva A, Bagshaw H, Baine M, et al. NCCN Guidelines(R) insights: Kidney cancer, Version 2.2024. J Natl Compr Canc Netw. 2024;22(1):4–16. https://doi.org/10.6004/jnccn.2024.0008
34. Bai J, Huang J, Ye Y, Lin J, Wen Y, Cai Z, et al. Clinicopathologic and prognosis of 30 patients with FH-deficient renal cell carcinoma: A single-center retrospective study. BMC Cancer. 2025;25(1):1152. https://doi.org/10.1186/s12885-025-14562-6
35. Motzer RJ, Tannir NM, McDermott DF, Aren Frontera O, Melichar B, Choueiri TK, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378(14):1277–90. https://doi.org/10.1056/NEJMoa1712126
36. Tannir NM, Albiges L, McDermott DF, Burotto M, Choueiri TK, Hammers HJ, et al. Nivolumab plus ipilimumab versus sunitinib for first-line treatment of advanced renal cell carcinoma: Extended 8-year follow-up results of efficacy and safety from the phase III CheckMate 214 trial. Ann Oncol. 2024;35(11):1026–38. https://doi.org/10.1016/j.annonc.2024.07.727
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Jun 1, 2026
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Pathologic Complete Response After Preoperative Ipilimumab and Nivolumab in an HLRCC Patient with Stage III RenalCell Carcinoma. (2026). Journal of Kidney Cancer, 13(2), 21-28. https://doi.org/10.15586/jkcvhl.v13i2.455
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Kidney Cancer: Case Reports
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Author Biography
Payal Kapur, Kidney Cancer Program at Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, Dallas, TX; Pathology, University of Texas Southwestern Medical Center, Dallas, TX, USA; Department of Urology, University of Texas Southwestern Medical Center, Dallas, TX
How to Cite
Pathologic Complete Response After Preoperative Ipilimumab and Nivolumab in an HLRCC Patient with Stage III RenalCell Carcinoma. (2026). Journal of Kidney Cancer, 13(2), 21-28. https://doi.org/10.15586/jkcvhl.v13i2.455