Incorporating Stereotactic Ablative Radiotherapy into the Multidisciplinary Management of Renal Cell Carcinoma
Abstract
:1. Introduction
2. Evidence Acquisition
3. Primary Localized RCC
- Renal mass biopsy. There is a high rate (31%) of benign pathology in resected renal masses [24]. An effort to reduce the morbidity of resecting benign renal masses has prompted increasing use of renal mass biopsy in patients with a small renal mass. A renal mass biopsy is diagnostic in 90% of small renal masses [25]. Utilization of biopsy prior to surgical resection is highly variable—it is likely most essential when a diagnosis other than renal cell carcinoma is suspected or biopsy results would impact the decision to proceed with treatment. A young patient unwilling to accept the uncertainties of a biopsy or a comorbid patient who would undergo active surveillance regardless of biopsy are good indications to avoid a biopsy [23]. Additional imaging with 99 mTc-sestamibi SPECT/CT [26] and 89Zr-DFO-girentuximab [27] are likely to become reasonable adjuncts to biopsy in the near future.
- Active surveillance is also increasingly utilized for small renal masses. Intermediate-term outcomes with this approach are excellent. The metastatic rate is generally low (<1–2%) in well-selected patients [28]. The DISSRM registry is a prospective active surveillance registry that has recently reported on 585 patients with a 3.39 year median follow-up [29]. The rate of delayed intervention on active surveillance is 15%, with no difference in cancer-specific survival between those that elected primary vs. delayed intervention. The most common reasons for intervention are growth rate >0.5 cm/year or patient preference [30].
- If treatment is elected, most patients are amenable to a robot-assisted partial nephrectomy. This has reduced morbidity over open partial nephrectomy and radical nephrectomy.
- Other local therapies. percutaneous ablation offers a reasonable alternative to surgery and can be performed with cryoablation or radiofrequency ablation [31]. A biopsy should confirm malignancy before ablation. This approach has reduced morbidity relative to surgery, which may be particularly relevant to the patient with elevated surgical risk. LC rates may be slightly lower than that of a partial nephrectomy, which is relevant to a patient with a long life expectancy.
- SABR. As discussed in the following sections, SABR is being increasingly considered.
3.1. SABR for Primary/Localized RCC
Author (Year) | Study Type | No. of Patients (N) | Follow-Up Duration (Months) | Dose (Gy)/No. of Fractions | Grade 3+ Toxicity (%) | Local Control (%) | Comments, Study Population |
---|---|---|---|---|---|---|---|
Grelier et al. (2021) [44] | Retrospective | 23 | 22 | 35/5–7 | 0 | 96 | Frail patients unfit for surgery or other ablative therapies |
Grubb et al. (2021) [49] | Prospective | 11 | 34.3 | 48/3 54/3 60/3 | 9.1 | 90 | Poor surgical candidates |
Swaminath et al. (2021) [45] | Prospective | 28 | NA | 30–42/ 3–5 | NA | NA | 13 patients ≤ 4 cm, 19 with >4 cm tumors |
Margulis et al. (2021) [50] | Prospective | 6 | 24 | 40/5 | 0 | NA | Neoadjuvant SABR for patients with IVC_TT |
Tetar et al. (2020) [48] | Retrospective | 36 | 16.4 | 40/5 | 0 | 95.2 | MRI-guided SABR, 31 patients had ≥T1b disease |
Siva et al. (2020) [47] | Retrospective | 95 | 32.4 | ____ | 0 | 97.1 | Large (>4 cm), T1b or higher tumors |
Senger et al. (2019) [43] | Retrospective | 10 | 27 | 24–25/1 36/3 | 0 | 92.3 | 7 with T1a and 3 with T3a disease |
Hannan et al. (2023) [51] | Prospective | 16 | 36 | 36/3 or 40/5 | 0 | 94 (1-year) | ≤5 cm enlarging primary RCC |
Siva et al. (2023) (FASTRACK II; Abstract only) [52] | Prospective | 70 | 42 | 26/1 (≤4 cm) 42/3 (>4 cm) | 10 | 100 | Non-surgical, T1b+ patients mostly |
3.2. SABR Dose Fractionation for Localized RCC
3.3. Response Evaluation after SABR
4. Locally Advanced RCC
4.1. Definitive Therapy with SABR for RCC with IVC Tumor Thrombus (IVC-TT)
4.2. Neoadjuvant SABR for RCC with IVC-TT
5. Metastatic RCC
- ○
- Karnofsky performance < 80%;
- ○
- Neutrophils > upper limit of normal;
- ○
- Corrected calcium > upper limit of normal;
- ○
- Platelets > upper limit of normal;
- ○
- Hemoglobin < lower limit of normal;
- ○
- <1 year from diagnosis to systemic therapy [66].
5.1. SABR for Metastatic RCC
5.2. SABR for Brain and Spinal Metastases
5.3. SABR for OM RCC
5.4. SABR for Oligoprogressive RCC
5.5. SABR for Primary Site Cytoreduction in mRCC
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
RCC | Renal Cell Carcinoma |
mRCC | Metastatic Renal Cell Carcinoma |
ICIs | Immune Checkpoint Inhibitors |
TKIs | Tyrosine Kinase Inhibitors |
SABR | Stereotactic Ablative Radiation Therapy |
RT | Radiation Therapy |
SRS | Stereotactic Radiosurgery |
IVC-TT | Inferior Vena Cava–Tumor Thrombus |
SPECT | Single-photon Emission Computed Tomography |
CT | Computed Tomography |
MRI | Magnetic Resonance Imaging |
DISSRM | Delayed Intervention and Surveillance for Small Renal Masses Registry |
IROCK | International Radiosurgery Consortium of the Kidney |
IMDC | International Metastatic Database Consortium |
LC | Local Control |
PFS | Progression-free Survival |
OS | Overall Survival |
CSS | Case-specific Survival |
HR | Hazard Ratio |
CIs | Confidence Intervals |
BED | Biological Effective Dose |
CR | Complete Response |
eGFR | estimated Glomerular Filtration Rate |
OM | Oligometastatic Disease |
OP | Oligoprogressive Disease |
BM | Brain Metastases |
WBRT | Whole-Brain Radiotherapy |
References
- Siegel, R.L.; Miller, K.D.; Wagle, N.S.; Jemal, A. Cancer Statistics, 2023. CA Cancer J. Clin. 2023, 73, 17–48. [Google Scholar] [CrossRef] [PubMed]
- Moch, H.; Amin, M.B.; Berney, D.M.; Compérat, E.M.; Gill, A.J.; Hartmann, A.; Menon, S.; Raspollini, M.R.; Rubin, M.A.; Srigley, J.R.; 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, 458–468. [Google Scholar] [CrossRef] [PubMed]
- Cozad, S.C.; Smalley, S.R.; Austenfeld, M.; Noble, M.; Jennings, S.; Raymond, R. Transitional Cell Carcinoma of the Renal Pelvis or Ureter: Patterns of Failure. Urology 1995, 46, 796–800. [Google Scholar] [CrossRef]
- Rabinovitch, R.A.; Zelefsky, M.J.; Gaynor, J.J.; Fuks, Z. Patterns of Failure Following Surgical Resection of Renal Cell Carcinoma: Implications for Adjuvant Local and Systemic Therapy. J. Clin. Oncol. 1994, 12, 206–212. [Google Scholar] [CrossRef] [PubMed]
- Choueiri, T.K.; Powles, T.; Burotto, M.; Escudier, B.; Bourlon, M.T.; Zurawski, B.; Oyervides Juárez, V.M.; Hsieh, J.J.; Basso, U.; Shah, A.Y.; et al. Nivolumab plus Cabozantinib versus Sunitinib for Advanced Renal-Cell Carcinoma. N. Engl. J. Med. 2021, 384, 829–841. [Google Scholar] [CrossRef] [PubMed]
- Motzer, R.; Alekseev, B.; Rha, S.-Y.; Porta, C.; Eto, M.; Powles, T.; Grünwald, V.; Hutson, T.E.; Kopyltsov, E.; Méndez-Vidal, M.J.; et al. Lenvatinib plus Pembrolizumab or Everolimus for Advanced Renal Cell Carcinoma. N. Engl. J. Med. 2021, 384, 1289–1300. [Google Scholar] [CrossRef]
- Motzer, R.J.; Penkov, K.; Haanen, J.; Rini, B.; Albiges, L.; Campbell, M.T.; Venugopal, B.; Kollmannsberger, C.; Negrier, S.; Uemura, M.; et al. Avelumab plus Axitinib versus Sunitinib for Advanced Renal-Cell Carcinoma. N. Engl. J. Med. 2019, 380, 1103–1115. [Google Scholar] [CrossRef] [PubMed]
- Deschavanne, P.J.; Fertil, B. A Review of Human Cell Radiosensitivity in Vitro. Int. J. Radiat. Oncol. 1996, 34, 251–266. [Google Scholar] [CrossRef]
- Walsh, L.; Stanfield, J.L.; Cho, L.C.; Chang, C.; Forster, K.; Kabbani, W.; Cadeddu, J.A.; Hsieh, J.-T.; Choy, H.; Timmerman, R.; et al. Efficacy of Ablative High-Dose-per-Fraction Radiation for Implanted Human Renal Cell Cancer in a Nude Mouse Model. Eur. Urol. 2006, 50, 795–800. [Google Scholar] [CrossRef]
- Ning, S.; Trisler, K.; Wessels, B.W.; Knox, S.J. Radiobiologic Studies of Radioimmunotherapy and External Beam Radiotherapy in Vitro and in Vivo in Human Renal Cell Carcinoma Xenografts. Cancer 1997, 80, 2519–2528. [Google Scholar] [CrossRef]
- Finkelstein, S.E.; Timmerman, R.; McBride, W.H.; Schaue, D.; Hoffe, S.E.; Mantz, C.A.; Wilson, G.D. The Confluence of Stereotactic Ablative Radiotherapy and Tumor Immunology. Clin. Dev. Immunol. 2011, 2011, 439752. [Google Scholar] [CrossRef]
- DiBiase, S.J.; Valicenti, R.K.; Schultz, D.; Xie, Y.; Gomella, L.G.; Corn, B.W. Palliative Irradiation for Focally Symptomatic Metastatic Renal Cell Carcinoma: Support for Dose Escalation Based on a Biological Model. J. Urol. 1997, 158, 746–749. [Google Scholar] [CrossRef]
- Wang, H.-H.; Cui, Y.-L.; Zaorsky, N.G.; Lan, J.; Deng, L.; Zeng, X.-L.; Wu, Z.-Q.; Tao, Z.; Guo, W.-H.; Wang, Q.-X.; et al. Mesenchymal Stem Cells Generate Pericytes to Promote Tumor Recurrence via Vasculogenesis after Stereotactic Body Radiation Therapy. Cancer Lett. 2016, 375, 349–359. [Google Scholar] [CrossRef]
- Ali, M.; Mooi, J.; Lawrentschuk, N.; McKay, R.R.; Hannan, R.; Lo, S.S.; Hall, W.A.; Siva, S. The Role of Stereotactic Ablative Body Radiotherapy in Renal Cell Carcinoma. Eur. Urol. 2022, 82, 613–622. [Google Scholar] [CrossRef]
- Chow, J.; Hoffend, N.C.; Abrams, S.I.; Schwaab, T.; Singh, A.K.; Muhitch, J.B. Radiation Induces Dynamic Changes to the T Cell Repertoire in Renal Cell Carcinoma Patients. Proc. Natl. Acad. Sci. USA 2020, 117, 23721–23729. [Google Scholar] [CrossRef] [PubMed]
- Potters, L.; Kavanagh, B.; Galvin, J.M.; Hevezi, J.M.; Janjan, N.A.; Larson, D.A.; Mehta, M.P.; Ryu, S.; Steinberg, M.; Timmerman, R.; et al. American Society for Therapeutic Radiology and Oncology (ASTRO) and American College of Radiology (ACR) Practice Guideline for the Performance of Stereotactic Body Radiation Therapy. Int. J. Radiat. Oncol. Biol. Phys. 2010, 76, 326–332. [Google Scholar] [CrossRef] [PubMed]
- Zelefsky, M.J.; Greco, C.; Motzer, R.; Magsanoc, J.M.; Pei, X.; Lovelock, M.; Mechalakos, J.; Zatcky, J.; Fuks, Z.; Yamada, Y. Tumor Control Outcomes after Hypofractionated and Single-Dose Stereotactic Image-Guided Intensity-Modulated Radiotherapy for Extracranial Metastases from Renal Cell Carcinoma. Int. J. Radiat. Oncol. 2012, 82, 1744–1748. [Google Scholar] [CrossRef] [PubMed]
- Svedman, C.; Sandström, P.; Pisa, P.; Blomgren, H.; Lax, I.; Kälkner, K.-M.; Nilsson, S.; Wersäll, P. A Prospective Phase II Trial of Using Extracranial Stereotactic Radiotherapy in Primary and Metastatic Renal Cell Carcinoma. Acta Oncol. 2006, 45, 870–875. [Google Scholar] [CrossRef] [PubMed]
- Wersäll, P.J.; Blomgren, H.; Lax, I.; Kälkner, K.-M.; Linder, C.; Lundell, G.; Nilsson, B.; Nilsson, S.; Näslund, I.; Pisa, P.; et al. Extracranial Stereotactic Radiotherapy for Primary and Metastatic Renal Cell Carcinoma. Radiother. Oncol. 2005, 77, 88–95. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.J.; Christie, A.; Lin, M.-H.; Jung, M.; Weix, D.; Huelsmann, L.; Kuhn, K.; Meyer, J.; Desai, N.; Kim, D.W.N.; et al. Safety and Efficacy of Stereotactic Ablative Radiation Therapy for Renal Cell Carcinoma Extracranial Metastases. Int. J. Radiat. Oncol. 2017, 98, 91–100. [Google Scholar] [CrossRef]
- Guidelines Detail. Available online: https://www.nccn.org/guidelines/guidelines-detail (accessed on 1 June 2023).
- Capitanio, U.; Bensalah, K.; Bex, A.; Boorjian, S.A.; Bray, F.; Coleman, J.; Gore, J.L.; Sun, M.; Wood, C.; Russo, P. Epidemiology of Renal Cell Carcinoma. Eur. Urol. 2019, 75, 74–84. [Google Scholar] [CrossRef] [PubMed]
- Campbell, S.C.; Clark, P.E.; Chang, S.S.; Karam, J.A.; Souter, L.; Uzzo, R.G. Renal Mass and Localized Renal Cancer: Evaluation, Management, and Follow-Up: AUA Guideline: Part I. J. Urol. 2021, 206, 199–208. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Li, S.; Khandwala, Y.; Chung, K.J.; Park, H.K.; Chung, B.I. Association of Prevalence of Benign Pathologic Findings after Partial Nephrectomy with Preoperative Imaging Patterns in the United States from 2007 to 2014. JAMA Surg. 2019, 154, 225–231. [Google Scholar] [CrossRef] [PubMed]
- Richard, P.O.; Jewett, M.A.S.; Bhatt, J.R.; Kachura, J.R.; Evans, A.J.; Zlotta, A.R.; Hermanns, T.; Juvet, T.; Finelli, A. Renal Tumor Biopsy for Small Renal Masses: A Single-Center 13-Year Experience. Eur. Urol. 2015, 68, 1007–1013. [Google Scholar] [CrossRef]
- Gorin, M.A.; Rowe, S.P.; Baras, A.S.; Solnes, L.B.; Ball, M.W.; Pierorazio, P.M.; Pavlovich, C.P.; Epstein, J.I.; Javadi, M.S.; Allaf, M.E. Prospective Evaluation of (99 m)Tc-Sestamibi SPECT/CT for the Diagnosis of Renal Oncocytomas and Hybrid Oncocytic/Chromophobe Tumors. Eur. Urol. 2016, 69, 413–416. [Google Scholar] [CrossRef]
- Shuch, B.M.; Pantuck, A.J.; Bernhard, J.-C.; Morris, M.A.; Master, V.A.; Scott, A.M.; Van Praet, C.; Bailly, C.; Aksoy, T.; Merkx, R.; et al. Results from Phase 3 Study of 89Zr-DFO-Girentuximab for PET/CT Imaging of Clear Cell Renal Cell Carcinoma (ZIRCON). J. Clin. Oncol. 2023, 41, LBA602. [Google Scholar] [CrossRef]
- Jewett, M.A.S.; Mattar, K.; Basiuk, J.; Morash, C.G.; Pautler, S.E.; Siemens, D.R.; Tanguay, S.; Rendon, R.A.; Gleave, M.E.; Drachenberg, D.E.; et al. Active Surveillance of Small Renal Masses: Progression Patterns of Early Stage Kidney Cancer. Eur. Urol. 2011, 60, 39–44. [Google Scholar] [CrossRef]
- Alkhatib, K.Y.; Cheaib, J.; Singla, N.; Chang, P.; Wagner, A.A.; Pavlovich, C.P.; Mckiernan, J.M.; Guzzo, T.J.; Allaf, M.E.; Pierorazio, P.M. PD08-11 active surveillance versus primary intervention for clinical t1a kidney tumors: Twelve-year experience of the dissrm prospective comparative study. J. Urol. 2023, 209, e237. [Google Scholar] [CrossRef]
- Gupta, M.; Alam, R.; Patel, H.D.; Semerjian, A.; Gorin, M.A.; Johnson, M.H.; Chang, P.; Wagner, A.A.; McKiernan, J.M.; Allaf, M.E.; et al. Use of Delayed Intervention for Small Renal Masses Initially Managed with Active Surveillance. Urol. Oncol. 2019, 37, 18–25. [Google Scholar] [CrossRef]
- Leopold, Z.; Passarelli, R.; Mikhail, M.; Tabakin, A.; Chua, K.; Ennis, R.D.; Nosher, J.; Singer, E.A. Modern Management of Localized Renal Cell Carcinoma-Is Ablation Part of the Equation? J. Kidney Cancer VHL 2022, 9, 5–23. [Google Scholar] [CrossRef]
- Frank, I.; Blute, M.L.; Cheville, J.C.; Lohse, C.M.; Weaver, A.L.; Zincke, H. Solid Renal Tumors: An Analysis of Pathological Features Related to Tumor Size. J. Urol. 2003, 170, 2217–2220. [Google Scholar] [CrossRef] [PubMed]
- Yanagisawa, T.; Mori, K.; Kawada, T.; Motlagh, R.S.; Mostafaei, H.; Quhal, F.; Laukhtina, E.; Rajwa, P.; Aydh, A.; König, F.; et al. Differential Efficacy of Ablation Therapy versus Partial Nephrectomy between Clinical T1a and T1b Renal Tumors: A Systematic Review and Meta-Analysis. Urol. Oncol. Semin. Orig. Investig. 2022, 40, 315–330. [Google Scholar] [CrossRef] [PubMed]
- Marzouk, K.; Tin, A.; Liu, N.; Sjoberg, D.; Hakimi, A.A.; Russo, P.; Coleman, J. The Natural History of Large Renal Masses Followed on Observation. Urol. Oncol. 2018, 36, 362.e17–362.e21. [Google Scholar] [CrossRef] [PubMed]
- Ljungberg, B.; Albiges, L.; Abu-Ghanem, Y.; Bedke, J.; Capitanio, U.; Dabestani, S.; Fernández-Pello, S.; Giles, R.H.; Hofmann, F.; Hora, M.; et al. European Association of Urology Guidelines on Renal Cell Carcinoma: The 2022 Update. Eur. Urol. 2022, 82, 399–410. [Google Scholar] [CrossRef] [PubMed]
- Escudier, B.; Porta, C.; Schmidinger, M.; Rioux-Leclercq, N.; Bex, A.; Khoo, V.; Grünwald, V.; Gillessen, S.; Horwich, A. Renal Cell Carcinoma: ESMO Clinical Practice Guidelines for Diagnosis, Treatment and Follow-Up. Ann. Oncol. 2019, 30, 706–720. [Google Scholar] [CrossRef]
- Sun, M.R.M.; Brook, A.; Powell, M.F.; Kaliannan, K.; Wagner, A.A.; Kaplan, I.D.; Pedrosa, I. Effect of Stereotactic Body Radiotherapy on the Growth Kinetics and Enhancement Pattern of Primary Renal Tumors. AJR Am. J. Roentgenol. 2016, 206, 544–553. [Google Scholar] [CrossRef]
- Ponsky, L.; Lo, S.S.; Zhang, Y.; Schluchter, M.; Liu, Y.; Patel, R.; Abouassaly, R.; Welford, S.; Gulani, V.; Haaga, J.R.; et al. Phase I Dose-Escalation Study of Stereotactic Body Radiotherapy (SBRT) for Poor Surgical Candidates with Localized Renal Cell Carcinoma. Radiother. Oncol. 2015, 117, 183–187. [Google Scholar] [CrossRef]
- Siva, S.; Pham, D.; Kron, T.; Bressel, M.; Lam, J.; Tan, T.H.; Chesson, B.; Shaw, M.; Chander, S.; Gill, S.; et al. Stereotactic Ablative Body Radiotherapy for Inoperable Primary Kidney Cancer: A Prospective Clinical Trial. BJU Int. 2017, 120, 623–630. [Google Scholar] [CrossRef]
- Correa, R.J.M.; Louie, A.V.; Zaorsky, N.G.; Lehrer, E.J.; Ellis, R.; Ponsky, L.; Kaplan, I.; Mahadevan, A.; Chu, W.; Swaminath, A.; et al. The Emerging Role of Stereotactic Ablative Radiotherapy for Primary Renal Cell Carcinoma: A Systematic Review and Meta-Analysis. Eur. Urol. Focus 2019, 5, 958–969. [Google Scholar] [CrossRef]
- Siva, S.; Louie, A.V.; Warner, A.; Muacevic, A.; Gandhidasan, S.; Ponsky, L.; Ellis, R.; Kaplan, I.; Mahadevan, A.; Chu, W.; et al. Pooled Analysis of Stereotactic Ablative Radiotherapy for Primary Renal Cell Carcinoma: A Report from the International Radiosurgery Oncology Consortium for Kidney (IROCK). Cancer 2018, 124, 934–942. [Google Scholar] [CrossRef]
- Siva, S.; Ali, M.; Correa, R.J.M.; Muacevic, A.; Ponsky, L.; Ellis, R.J.; Lo, S.S.; Onishi, H.; Swaminath, A.; McLaughlin, M.; et al. 5-Year Outcomes after Stereotactic Ablative Body Radiotherapy for Primary Renal Cell Carcinoma: An Individual Patient Data Meta-Analysis from IROCK (the International Radiosurgery Consortium of the Kidney). Lancet Oncol. 2022, 23, 1508–1516. [Google Scholar] [CrossRef]
- Senger, C.; Conti, A.; Kluge, A.; Pasemann, D.; Kufeld, M.; Acker, G.; Lukas, M.; Grün, A.; Kalinauskaite, G.; Budach, V.; et al. Robotic Stereotactic Ablative Radiotherapy for Renal Cell Carcinoma in Patients with Impaired Renal Function. BMC Urol. 2019, 19, 96. [Google Scholar] [CrossRef]
- Grelier, L.; Baboudjian, M.; Gondran-Tellier, B.; Couderc, A.-L.; McManus, R.; Deville, J.-L.; Carballeira, A.; Delonca, R.; Delaporte, V.; Padovani, L.; et al. Stereotactic Body Radiotherapy for Frail Patients with Primary Renal Cell Carcinoma: Preliminary Results after 4 Years of Experience. Cancers 2021, 13, 3129. [Google Scholar] [CrossRef]
- Swaminath, A.; Cheung, P.; Glicksman, R.M.; Donovan, E.K.; Niglas, M.; Vesprini, D.; Kapoor, A.; Erler, D.; Chu, W. Patient-Reported Quality of Life Following Stereotactic Body Radiation Therapy for Primary Kidney Cancer—Results from a Prospective Cohort Study. Clin. Oncol. 2021, 33, 468–475. [Google Scholar] [CrossRef]
- Abboud, S.E.; Patel, T.; Soriano, S.; Giesler, J.; Alvarado, N.; Kang, P. Long-Term Clinical Outcomes Following Radiofrequency and Microwave Ablation of Renal Cell Carcinoma at a Single VA Medical Center. Curr. Probl. Diagn. Radiol. 2018, 47, 98–102. [Google Scholar] [CrossRef]
- Siva, S.; Correa, R.J.M.; Warner, A.; Staehler, M.; Ellis, R.J.; Ponsky, L.; Kaplan, I.D.; Mahadevan, A.; Chu, W.; Gandhidasan, S.; et al. Stereotactic Ablative Radiotherapy for ≥T1b Primary Renal Cell Carcinoma: A Report From the International Radiosurgery Oncology Consortium for Kidney (IROCK). Int. J. Radiat. Oncol. 2020, 108, 941–949. [Google Scholar] [CrossRef]
- Tetar, S.U.; Bohoudi, O.; Senan, S.; Palacios, M.A.; Oei, S.S.; van der Wel, A.M.; Slotman, B.J.; van Moorselaar, R.J.A.; Lagerwaard, F.J.; Bruynzeel, A.M.E. The Role of Daily Adaptive Stereotactic MR-Guided Radiotherapy for Renal Cell Cancer. Cancers 2020, 12, 2763. [Google Scholar] [CrossRef]
- Grubb, W.R.; Ponsky, L.; Lo, S.S.; Kharouta, M.; Traughber, B.; Sandstrom, K.; MacLennan, G.T.; Shankar, E.; Gupta, S.; Machtay, M.; et al. Final Results of a Dose Escalation Protocol of Stereotactic Body Radiotherapy for Poor Surgical Candidates with Localized Renal Cell Carcinoma. Radiother. Oncol. 2021, 155, 138–143. [Google Scholar] [CrossRef]
- Siva, S.; Chesson, B.; Bressel, M.; Pryor, D.; Higgs, B.; Reynolds, H.M.; Hardcastle, N.; Montgomery, R.; Vanneste, B.; Khoo, V.; et al. TROG 15.03 Phase II Clinical Trial of Focal Ablative STereotactic Radiosurgery for Cancers of the Kidney—FASTRACK II. BMC Cancer 2018, 18, 1030. [Google Scholar] [CrossRef]
- Siva, S.; Ellis, R.J.; Ponsky, L.; Teh, B.S.; Mahadevan, A.; Muacevic, A.; Staehler, M.; Onishi, H.; Wersall, P.; Nomiya, T.; et al. Consensus Statement from the International Radiosurgery Oncology Consortium for Kidney for Primary Renal Cell Carcinoma. Future Oncol. 2016, 12, 637–645. [Google Scholar] [CrossRef]
- Ray, S.; Dason, S.; Singer, E.A. Integrating Surgery in the Multidisciplinary Care of Advanced Renal Cell Carcinoma. Urol. Clin. N. Am. 2023, 50, 311–323. [Google Scholar] [CrossRef]
- Choueiri, T.K.; Tomczak, P.; Park, S.H.; Venugopal, B.; Ferguson, T.; Chang, Y.-H.; Hajek, J.; Symeonides, S.N.; Lee, J.L.; Sarwar, N.; et al. Adjuvant Pembrolizumab after Nephrectomy in Renal-Cell Carcinoma. N. Engl. J. Med. 2021, 385, 683–694. [Google Scholar] [CrossRef]
- Powles, T.; Tomczak, P.; Park, S.H.; Venugopal, B.; Ferguson, T.; Symeonides, S.N.; Hajek, J.; Gurney, H.; Chang, Y.-H.; Lee, J.L.; et al. Pembrolizumab versus Placebo as Post-Nephrectomy Adjuvant Therapy for Clear Cell Renal Cell Carcinoma (KEYNOTE-564): 30-Month Follow-up Analysis of a Multicentre, Randomised, Double-Blind, Placebo-Controlled, Phase 3 Trial. Lancet Oncol. 2022, 23, 1133–1144. [Google Scholar] [CrossRef] [PubMed]
- Margulis, V.; Freifeld, Y.; Pop, L.M.; Manna, S.; Kapur, P.; Pedrosa, I.; Christie, A.; Mohamad, O.; Mannala, S.; Singla, N.; et al. Neoadjuvant SABR for Renal Cell Carcinoma Inferior Vena Cava Tumor Thrombus-Safety Lead-in Results of a Phase 2 Trial. Int. J. Radiat. Oncol. Biol. Phys. 2021, 110, 1135–1142. [Google Scholar] [CrossRef]
- Hannan, R.; McLaughlin, M.F.; Pop, L.M.; Pedrosa, I.; Kapur, P.; Garant, A.; Ahn, C.; Christie, A.; Zhu, J.; Wang, T.; et al. Phase 2 Trial of Stereotactic Ablative Radiotherapy for Patients with Primary Renal Cancer. Eur. Urol. 2023, 84, 275–286. [Google Scholar] [CrossRef] [PubMed]
- Siva, S.; Bressel, M.; Sidhom, M.; Sridharan, S.; Vanneste, B.; Davey, R.; Ruben, J.; Foroudi, F.; Higgs, B.G.; Lin, C.; et al. TROG 15.03/ANZUP International Multicenter Phase II Trial of Focal Ablative STereotactic RAdiotherapy for Cancers of the Kidney (FASTRACK II). Int. J. Radiat. Oncol. Biol. Phys. 2023, 117, S3. [Google Scholar] [CrossRef]
- Reese, A.C.; Whitson, J.M.; Meng, M.V. Natural History of Untreated Renal Cell Carcinoma with Venous Tumor Thrombus. Urol. Oncol. 2013, 31, 1305–1309. [Google Scholar] [CrossRef]
- Christensen, M.; Hannan, R. The Emerging Role of Radiation Therapy in Renal Cell Carcinoma. Cancers 2022, 14, 4693. [Google Scholar] [CrossRef] [PubMed]
- Hannan, R.; Margulis, V.; Chun, S.G.; Cannon, N.; Kim, D.W.N.; Abdulrahman, R.E.; Sagalowsky, A.; Pedrosa, I.; Choy, H.; Brugarolas, J.; et al. Stereotactic Radiation Therapy of Renal Cancer Inferior Vena Cava Tumor Thrombus. Cancer Biol. Ther. 2015, 16, 657–661. [Google Scholar] [CrossRef]
- Freifeld, Y.; Pedrosa, I.; Mclaughlin, M.; Correa, R.M.; Louie, A.V.; Maldonado, J.A.; Tang, C.; Kadow, B.; Kutikov, A.; Uzzo, R.G.; et al. Stereotactic Ablative Radiation Therapy for Renal Cell Carcinoma with Inferior Vena Cava Tumor Thrombus. Urol. Oncol. 2022, 40, 166.e9–166.e13. [Google Scholar] [CrossRef]
- Freifeld, Y.; Margulis, V.; Woldu, S.L.; Timmerman, R.; Brugarolas, J.; Hannan, R. Stereotactic Body Radiation Therapy for Renal Cell Carcinoma with Inferior Vena Cava Thrombus—Initial Experience Report and Literature Review. Kidney Cancer 2019, 3, 71–77. [Google Scholar] [CrossRef]
- Chen, Z.; Yang, F.; Ge, L.; Qiu, M.; Liu, Z.; Liu, C.; Tian, X.; Zhang, S.; Ma, L. Outcomes of Renal Cell Carcinoma with Associated Venous Tumor Thrombus: Experience from a Large Cohort and Short Time Span in a Single Center. BMC Cancer 2021, 21, 766. [Google Scholar] [CrossRef]
- Ray, S.; Singer, E.A.; Dason, S. Inferior Vena Cava Thrombectomy for Renal Cell Carcinoma: Perioperative Systemic Therapy, Cytoreductive Nephrectomy, and Complex Cases. Ann. Transl. Med. 2023, 11, 239. [Google Scholar] [CrossRef]
- Dason, S.; Mohebali, J.; Blute, M.L.; Salari, K. Surgical Management of Renal Cell Carcinoma with Inferior Vena Cava Tumor Thrombus. Urol. Clin. N. Am. 2023, 50, 261–284. [Google Scholar] [CrossRef]
- Heng, D.Y.C.; Xie, W.; Regan, M.M.; Harshman, L.C.; Bjarnason, G.A.; Vaishampayan, U.N.; Mackenzie, M.; Wood, L.; Donskov, F.; Tan, M.-H.; et al. External Validation and Comparison with Other Models of the International Metastatic Renal-Cell Carcinoma Database Consortium Prognostic Model: A Population-Based Study. Lancet Oncol. 2013, 14, 141–148. [Google Scholar] [CrossRef]
- Liu, Y.; Zhang, Z.; Han, H.; Guo, S.; Liu, Z.; Liu, M.; Zhou, F.; Dong, P.; He, L. Survival After Combining Stereotactic Body Radiation Therapy and Tyrosine Kinase Inhibitors in Patients with Metastatic Renal Cell Carcinoma. Front. Oncol. 2021, 11, 607595. [Google Scholar] [CrossRef]
- Rathmell, W.K.; Rumble, R.B.; Van Veldhuizen, P.J.; Al-Ahmadie, H.; Emamekhoo, H.; Hauke, R.J.; Louie, A.V.; Milowsky, M.I.; Molina, A.M.; Rose, T.L.; et al. Management of Metastatic Clear Cell Renal Cell Carcinoma: ASCO Guideline. J. Clin. Oncol. 2022, 40, 2957–2995. [Google Scholar] [CrossRef]
- Dason, S.; Lacuna, K.; Hannan, R.; Singer, E.A.; Runcie, K. State of the Art: Multidisciplinary Management of Oligometastatic Renal Cell Carcinoma. Am. Soc. Clin. Oncol. Educ. Book 2023, 43, e390038. [Google Scholar] [CrossRef] [PubMed]
- Andrews, J.R.; Lohse, C.M.; Boorjian, S.A.; Leibovich, B.C.; Thompson, H.; Costello, B.A.; Bhindi, B. Outcomes Following Cytoreductive Nephrectomy without Immediate Postoperative Systemic Therapy for Patients with Synchronous Metastatic Renal Cell Carcinoma. Urol. Oncol. 2022, 40, 166.e1–166.e8. [Google Scholar] [CrossRef] [PubMed]
- Rini, B.I.; Dorff, T.B.; Elson, P.; Rodriguez, C.S.; Shepard, D.; Wood, L.; Humbert, J.; Pyle, L.; Wong, Y.-N.; Finke, J.H.; et al. Active Surveillance in Metastatic Renal-Cell Carcinoma: A Prospective, Phase 2 Trial. Lancet Oncol. 2016, 17, 1317–1324. [Google Scholar] [CrossRef] [PubMed]
- Lyon, T.D.; Thompson, R.H.; Shah, P.H.; Lohse, C.M.; Boorjian, S.A.; Costello, B.A.; Cheville, J.C.; Leibovich, B.C. Complete Surgical Metastasectomy of Renal Cell Carcinoma in the Post-Cytokine Era. J. Urol. 2020, 203, 275–282. [Google Scholar] [CrossRef] [PubMed]
- Zaorsky, N.G.; Lehrer, E.J.; Kothari, G.; Louie, A.V.; Siva, S. Stereotactic Ablative Radiation Therapy for Oligometastatic Renal Cell Carcinoma (SABR ORCA): A Meta-Analysis of 28 Studies. Eur. Urol. Oncol. 2019, 2, 515–523. [Google Scholar] [CrossRef]
- Dengina, N.; Mitin, T.; Gamayunov, S.; Safina, S.; Kreinina, Y.; Tsimafeyeu, I. Stereotactic Body Radiation Therapy in Combination with Systemic Therapy for Metastatic Renal Cell Carcinoma: A Prospective Multicentre Study. ESMO Open 2019, 4, e000535. [Google Scholar] [CrossRef] [PubMed]
- Masini, C.; Iotti, C.; De Giorgi, U.; Bellia, R.S.; Buti, S.; Salaroli, F.; Zampiva, I.; Mazzarotto, R.; Mucciarini, C.; Baldessari, C.; et al. Nivolumab (NIVO) in Combination with Stereotactic Body Radiotherapy (SBRT) in Pretreated Patients (Pts) with Metastatic Renal Cell Carcinoma (mRCC): First Results of Phase II NIVES Study. J. Clin. Oncol. 2020, 38, 613. [Google Scholar] [CrossRef]
- Hannan, R.; Mohamad, O.; Diaz de Leon, A.; Manna, S.; Pop, L.M.; Zhang, Z.; Mannala, S.; Christie, A.; Christley, S.; Monson, N.; et al. Outcome and Immune Correlates of a Phase II Trial of High-Dose Interleukin-2 and Stereotactic Ablative Radiotherapy for Metastatic Renal Cell Carcinoma. Clin. Cancer Res. 2021, 27, 6716–6725. [Google Scholar] [CrossRef] [PubMed]
- Hammers, H.J.; Vonmerveldt, D.; Ahn, C.; Nadal, R.M.; Drake, C.G.; Folkert, M.R.; Laine, A.M.; Courtney, K.D.; Brugarolas, J.; Song, D.Y.; et al. Combination of Dual Immune Checkpoint Inhibition (ICI) with Stereotactic Radiation (SBRT) in Metastatic Renal Cell Carcinoma (mRCC) (RADVAX RCC). J. Clin. Oncol. 2020, 38, 614. [Google Scholar] [CrossRef]
- Siva, S.; Bressel, M.; Wood, S.T.; Shaw, M.G.; Loi, S.; Sandhu, S.K.; Tran, B.; Azad, A.A.; Lewin, J.H.; Cuff, K.E.; et al. Stereotactic Radiotherapy and Short-Course Pembrolizumab for Oligometastatic Renal Cell Carcinoma—The RAPPORT Trial. Eur. Urol. 2022, 81, 364–372. [Google Scholar] [CrossRef]
- Hirsch, L.; Martinez Chanza, N.; Farah, S.; Xie, W.; Flippot, R.; Braun, D.A.; Rathi, N.; Thouvenin, J.; Collier, K.A.; Seront, E.; et al. Clinical Activity and Safety of Cabozantinib for Brain Metastases in Patients With Renal Cell Carcinoma. JAMA Oncol. 2021, 7, 1815–1823. [Google Scholar] [CrossRef]
- Flippot, R.; Dalban, C.; Laguerre, B.; Borchiellini, D.; Gravis, G.; Négrier, S.; Chevreau, C.; Joly, F.; Geoffrois, L.; Ladoire, S.; et al. Safety and Efficacy of Nivolumab in Brain Metastases From Renal Cell Carcinoma: Results of the GETUG-AFU 26 NIVOREN Multicenter Phase II Study. J. Clin. Oncol. 2019, 37, 2008–2016. [Google Scholar] [CrossRef]
- Chang, E.L.; Wefel, J.S.; Hess, K.R.; Allen, P.K.; Lang, F.F.; Kornguth, D.G.; Arbuckle, R.B.; Swint, J.M.; Shiu, A.S.; Maor, M.H.; et al. Neurocognition in Patients with Brain Metastases Treated with Radiosurgery or Radiosurgery plus Whole-Brain Irradiation: A Randomised Controlled Trial. Lancet Oncol. 2009, 10, 1037–1044. [Google Scholar] [CrossRef]
- Ko, J.J.; Xie, W.; Kroeger, N.; Lee, J.; Rini, B.I.; Knox, J.J.; Bjarnason, G.A.; Srinivas, S.; Pal, S.K.; Yuasa, T.; et al. The International Metastatic Renal Cell Carcinoma Database Consortium Model as a Prognostic Tool in Patients with Metastatic Renal Cell Carcinoma Previously Treated with First-Line Targeted Therapy: A Population-Based Study. Lancet Oncol. 2015, 16, 293–300. [Google Scholar] [CrossRef]
- Smith, B.W.; Joseph, J.R.; Saadeh, Y.S.; La Marca, F.; Szerlip, N.J.; Schermerhorn, T.C.; Spratt, D.E.; Younge, K.C.; Park, P. Radiosurgery for Treatment of Renal Cell Metastases to Spine: A Systematic Review of the Literature. World Neurosurg. 2018, 109, e502–e509. [Google Scholar] [CrossRef] [PubMed]
- Laufer, I.; Iorgulescu, J.B.; Chapman, T.; Lis, E.; Shi, W.; Zhang, Z.; Cox, B.W.; Yamada, Y.; Bilsky, M.H. Local Disease Control for Spinal Metastases Following “Separation Surgery” and Adjuvant Hypofractionated or High-Dose Single-Fraction Stereotactic Radiation Therapy: Outcomes Analysis in 186 Patients. J. Neurosurg. Spine 2013, 18, 207–214. [Google Scholar] [CrossRef] [PubMed]
- Hussain, I.; Goldberg, J.L.; Carnevale, J.A.; Hanz, S.Z.; Reiner, A.S.; Schmitt, A.; Higginson, D.S.; Yamada, Y.; Laufer, I.; Bilsky, M.H.; et al. Hybrid Therapy (Surgery and Radiosurgery) for the Treatment of Renal Cell Carcinoma Spinal Metastases. Neurosurgery 2022, 90, 199. [Google Scholar] [CrossRef] [PubMed]
- Paciotti, M.; Schmidt, A.L.; Ravi, P.; McKay, R.R.; Trinh, Q.; Choueiri, T.K. Temporal Trends and Predictors in the Use of Stereotactic Body Radiotherapy for Treatment of Metastatic Renal Cell Carcinoma in the U.S. Oncologist 2021, 26, e905–e906. [Google Scholar] [CrossRef] [PubMed]
- Turgeon, G.-A.; Weickhardt, A.; Azad, A.A.; Solomon, B.; Siva, S. Radiotherapy and Immunotherapy: A Synergistic Effect in Cancer Care. Med. J. Aust. 2019, 210, 47–53. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.; Msaouel, P.; Hara, K.; Choi, H.; Le, V.; Shah, A.Y.; Wang, J.; Jonasch, E.; Choi, S.; Nguyen, Q.; et al. Definitive Radiotherapy in Lieu of Systemic Therapy for Oligometastatic Renal Cell Carcinoma: A Single-Arm, Single-Centre, Feasibility, Phase 2 Trial. Lancet Oncol. 2021, 22, 1732–1739. [Google Scholar] [CrossRef] [PubMed]
- Hannan, R.; Christensen, M.; Christie, A.; Garant, A.; Pedrosa, I.; Robles, L.; Mannala, S.; Wang, C.; Hammers, H.; Arafat, W.; et al. Stereotactic Ablative Radiation for Systemic Therapy-Naïve Oligometastatic Kidney Cancer. Eur. Urol. Oncol. 2022, 5, 695–703. [Google Scholar] [CrossRef]
- Chalkidou, A.; Macmillan, T.; Grzeda, M.T.; Peacock, J.; Summers, J.; Eddy, S.; Coker, B.; Patrick, H.; Powell, H.; Berry, L.; et al. Stereotactic Ablative Body Radiotherapy in Patients with Oligometastatic Cancers: A Prospective, Registry-Based, Single-Arm, Observational, Evaluation Study. Lancet Oncol. 2021, 22, 98–106. [Google Scholar] [CrossRef]
- Cao, G.; Wu, X.; Wang, Z.; Tian, X.; Zhang, C.; Wu, X.; Zhang, H.; Jing, G.; Yan, T. What Is the Optimum Systemic Treatment for Advanced/Metastatic Renal Cell Carcinoma of Favourable, Intermediate and Poor Risk, Respectively? A Systematic Review and Network Meta-Analysis. BMJ Open 2020, 10, e034626. [Google Scholar] [CrossRef]
- Guillaume, E.; Tanguy, R.; Ayadi, M.; Claude, L.; Sotton, S.; Moncharmont, C.; Magné, N.; Martel-Lafay, I. Toxicity and Efficacy of Stereotactic Body Radiotherapy for Ultra-Central Lung Tumours: A Single Institution Real Life Experience. Br. J. Radiol. 2022, 95, 20210533. [Google Scholar] [CrossRef] [PubMed]
- Kroeze, S.G.C.; Fritz, C.; Schaule, J.; Siva, S.; Kahl, K.H.; Sundahl, N.; Blanck, O.; Kaul, D.; Adebahr, S.; Verhoeff, J.J.C.; et al. Stereotactic Radiotherapy Combined with Immunotherapy or Targeted Therapy for Metastatic Renal Cell Carcinoma. BJU Int. 2021, 127, 703–711. [Google Scholar] [CrossRef] [PubMed]
- He, L.; Liu, Y.; Han, H.; Liu, Z.; Huang, S.; Cao, W.; Liu, B.; Qin, Z.; Guo, S.; Zhang, Z.; et al. Survival Outcomes after Adding Stereotactic Body Radiotherapy to Metastatic Renal Cell Carcinoma Patients Treated with Tyrosine Kinase Inhibitors. Am. J. Clin. Oncol. 2020, 43, 58–63. [Google Scholar] [CrossRef]
- Buti, S.; Bersanelli, M.; Viansone, A.; Leonetti, A.; Masini, C.; Ratta, R.; Procopio, G.; Maines, F.; Iacovelli, R.; Ciccarese, C.; et al. Treatment Outcome of Metastatic Lesions from Renal Cell Carcinoma underGoing Extra-Cranial Stereotactic Body radioTHERapy: The Together Retrospective Study. Cancer Treat. Res. Commun. 2020, 22, 100161. [Google Scholar] [CrossRef]
- Franzese, C.; Marvaso, G.; Francolini, G.; Borghetti, P.; Trodella, L.E.; Sepulcri, M.; Matrone, F.; Nicosia, L.; Timon, G.; Ognibene, L.; et al. The Role of Stereotactic Body Radiation Therapy and Its Integration with Systemic Therapies in Metastatic Kidney Cancer: A Multicenter Study on Behalf of the AIRO (Italian Association of Radiotherapy and Clinical Oncology) Genitourinary Study Group. Clin. Exp. Metastasis 2021, 38, 527–537. [Google Scholar] [CrossRef]
- Cheung, P.; Patel, S.; North, S.A.; Sahgal, A.; Chu, W.; Soliman, H.; Ahmad, B.; Winquist, E.; Niazi, T.; Patenaude, F.; et al. Stereotactic Radiotherapy for Oligoprogression in Metastatic Renal Cell Cancer Patients Receiving Tyrosine Kinase Inhibitor Therapy: A Phase 2 Prospective Multicenter Study. Eur. Urol. 2021, 80, 693–700. [Google Scholar] [CrossRef] [PubMed]
- Flanigan, R.C.; Salmon, S.E.; Blumenstein, B.A.; Bearman, S.I.; Roy, V.; McGrath, P.C.; Caton, J.R.; Munshi, N.; Crawford, E.D. Nephrectomy Followed by Interferon Alfa-2b Compared with Interferon Alfa-2b Alone for Metastatic Renal-Cell Cancer. N. Engl. J. Med. 2001, 345, 1655–1659. [Google Scholar] [CrossRef] [PubMed]
- Mickisch, G.H.; Garin, A.; van Poppel, H.; de Prijck, L.; Sylvester, R.; European Organisation for Research and Treatment of Cancer (EORTC) Genitourinary Group. Radical Nephrectomy plus Interferon-Alfa-Based Immunotherapy Compared with Interferon Alfa Alone in Metastatic Renal-Cell Carcinoma: A Randomised Trial. Lancet 2001, 358, 966–970. [Google Scholar] [CrossRef]
- Méjean, A.; Ravaud, A.; Thezenas, S.; Colas, S.; Beauval, J.-B.; Bensalah, K.; Geoffrois, L.; Thiery-Vuillemin, A.; Cormier, L.; Lang, H.; et al. Sunitinib Alone or after Nephrectomy in Metastatic Renal-Cell Carcinoma. N. Engl. J. Med. 2018, 379, 417–427. [Google Scholar] [CrossRef] [PubMed]
1. Not a candidate for surgery due to perioperative risk, patient preference, or equipoise on benefit of surgery in context of disease burden. And 2. One or more of:
|
|
1. Metachronous metastases (>1 year after resection of primary renal tumor) | Indolent disease; best prognosis |
|
2. IMDC favorable or intermediate risk | High risk of occult micrometastases |
|
3. IMDC high risk, grade 4 or sarcomatoid component histology | High risk of occult micrometastatic disease with anticipated rapid progression |
|
Primary localized or locally advanced RCC |
|
Metastatic RCC |
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Raj, R.K.; Upadhyay, R.; Wang, S.-J.; Singer, E.A.; Dason, S. Incorporating Stereotactic Ablative Radiotherapy into the Multidisciplinary Management of Renal Cell Carcinoma. Curr. Oncol. 2023, 30, 10283-10298. https://doi.org/10.3390/curroncol30120749
Raj RK, Upadhyay R, Wang S-J, Singer EA, Dason S. Incorporating Stereotactic Ablative Radiotherapy into the Multidisciplinary Management of Renal Cell Carcinoma. Current Oncology. 2023; 30(12):10283-10298. https://doi.org/10.3390/curroncol30120749
Chicago/Turabian StyleRaj, Rohit K., Rituraj Upadhyay, Shang-Jui Wang, Eric A. Singer, and Shawn Dason. 2023. "Incorporating Stereotactic Ablative Radiotherapy into the Multidisciplinary Management of Renal Cell Carcinoma" Current Oncology 30, no. 12: 10283-10298. https://doi.org/10.3390/curroncol30120749