Augmenting the Randomized Controlled Trial with Real-World Data to Aid Clinical Decision Making in Metastatic Renal Cell Carcinoma: A Systematic Review and Meta-Analysis

References

• Rothwell PM . Commentary: external validity of results of randomized trials: disentangling a complex concept. Int. J. Epidemiol.39(1), 94–96 (2010).
   PubMed Web of Science ®Google Scholar
• Sherman RE , AndersonSA, DalPan GJet al. Real-world evidence – what is it and what can it tell us?N. Engl. J. Med.375(23), 2293–2297 (2016).
   PubMed Web of Science ®Google Scholar
• Rothwell PM . External validity of randomised controlled trials: ‘to whom do the results of this trial apply?’. Lancet365(9453), 82–93 (2005).
   PubMed Web of Science ®Google Scholar
• Van Spall HG , TorenA, KissA, FowlerRA. Eligibility criteria of randomized controlled trials published in high-impact general medical journals: a systematic sampling review. JAMA297(11), 1233–1240 (2007).
   PubMed Web of Science ®Google Scholar
• Khozin S , BlumenthalGM, PazdurR. Real-world data for clinical evidence generation in oncology. J. Natl Cancer Inst.109(11), (2017). doi:10.1093/jnci/djx187
   PubMedGoogle Scholar
• Association of the British Pharmaceutical Industry . The vision for real world data – harnessing the opportunities in the UK (2011). http://www.abpi.org.uk/publications/vision-for-real-world-data
   Google Scholar
• McDonald L , LambrelliD, WasiakR, RamagopalanSV. Real-world data in the United Kingdom: opportunities and challenges. BMC Med.14(1), 97 (2016).
   PubMedGoogle Scholar
• Argyropulo-Palmer M , JenkinsA, ThetiDS, LarkinJ, MontgomeryD. Sunitinib in metastatic renal cell carcinoma: a systematic review of UK real world data. Front. Oncol.5, 195 (2015).
   PubMed Web of Science ®Google Scholar
• Katkade VB , SandersKN, ZouKH. Real world data: an opportunity to supplement existing evidence for the use of long-established medicines in health care decision making. J. Multidiscip. Healthc.11, 295–304 (2018).
   PubMed Web of Science ®Google Scholar
• Murthy VH , KrumholzHM, GrossCP. Participation in cancer clinical trials: race-, sex-, and age-based disparities. JAMA291(22), 2720–2726 (2004).
   PubMed Web of Science ®Google Scholar
• Dias AL , ChaoJH, LeeD, WuY, KloeckerGH. Patient perceptions concerning clinical trials in oncology patients. Contemp. Clin. Trials Commun.4, 179–185 (2016).
   PubMedGoogle Scholar
• Schroen AT , PetroniGR, WangHet al. Preliminary evaluation of factors associated with premature trial closure and feasibility of accrual benchmarks in Phase III oncology trials. Clin. Trials7(4), 312–321 (2010).
   PubMed Web of Science ®Google Scholar
• American Society of Clinical Oncology (ASCO) and Friends of Cancer Research . Cancer clinical trial eligibility criteria (2018). https://www.focr.org/sites/default/files/pdf/ASCO-Friends%20Cancer%20Clinical%20Trials%20Eligibility%20Criteria_Aug_8_2018_0.pdf
   Google Scholar
• Bray F , FerlayJ, SoerjomataramI, SiegelRL, TorreLA, JemalA. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.68(6), 394–424 (2018).
   PubMed Web of Science ®Google Scholar
• National Comprehensive Cancer Network . NCCN clinical practice guidelines in oncology: kidney cancer. Version 3 (2019). https://www.nccn.org/professionals/physician_gls/default.aspx#site
   Google Scholar
• Dabestani S , ThorstensonA, LindbladP, HarmenbergU, LjungbergB, LundstamS. Renal cell carcinoma recurrences and metastases in primary non-metastatic patients: a population-based study. World J. Urol.34(8), 1081–1086 (2016).
   PubMed Web of Science ®Google Scholar
• Escudier B , PortaC, SchmidingerMet al. Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol.30(5), 706–720 (2019).
   PubMed Web of Science ®Google Scholar
• European Association of Urology. Renal cell carcinoma guidelines (2019). https://uroweb.org/guideline/renal-cell-carcinoma/
   Google Scholar
• The American Cancer Society . Survival rates for kidney cancer by stage (31 January 2019). http://www.cancer.org/cancer/kidney-cancer/detection-diagnosis-staging/survival-rates.html
   Google Scholar
• Zarrabi K , FangC, WuS. New treatment options for metastatic renal cell carcinoma with prior anti-angiogenesis therapy. J. Hematol. Oncol.10(1), 38 (2017).
   PubMedGoogle Scholar
• Liberati A , AltmanDG, TetzlaffJet al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J. Clin. Epidemiol.62(10), e1–34 (2009).
   PubMed Web of Science ®Google Scholar
• Morrison A , PolisenaJ, HusereauDet al. The effect of English-language restriction on systematic review-based meta-analyses: a systematic review of empirical studies. Int. J. Technol. Assess. Health Care28(2), 138–144 (2012).
   PubMed Web of Science ®Google Scholar
• Moran M , NickensD, AdcockKet al. Sunitinib for metastatic renal cell carcinoma: a systematic review and meta-analysis of real-world and clinical trials data. Target Oncol.14(4), 405–416 (2019).
   PubMed Web of Science ®Google Scholar
• Armstrong AJ , HalabiS, EisenTet al. Everolimus versus sunitinib for patients with metastatic non-clear cell renal cell carcinoma (ASPEN): a multicentre, open-label, randomised Phase II trial. Lancet Oncol.17(3), 378–388 (2016).
   PubMed Web of Science ®Google Scholar
• Choueiri TK , HalabiS, SanfordBLet al. Cabozantinib versus sunitinib as initial targeted therapy for patients with metastatic renal cell carcinoma of poor or intermediate risk: The Alliance A031203 CABOSUN Trial. J. Clin. Oncol.35(6), 591–597 (2017).
   PubMed Web of Science ®Google Scholar
• Escudier B , SzczylikC, HutsonTEet al. Randomized Phase II trial of first-line treatment with sorafenib versus interferon α-2a in patients with metastatic renal cell carcinoma. J. Clin. Oncol.27(8), 1280–1289 (2009).
   PubMed Web of Science ®Google Scholar
• Hutson TE , LesovoyV, Al-ShukriSet al. Axitinib versus sorafenib as first-line therapy in patients with metastatic renal-cell carcinoma: a randomised open-label Phase III trial. Lancet Oncol.14(13), 1287–1294 (2013).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , BarriosCH, KimTMet al. Phase II randomized trial comparing sequential first-line everolimus and second-line sunitinib versus first-line sunitinib and second-line everolimus in patients with metastatic renal cell carcinoma. J. Clin. Oncol.32(25), 2765–2772 (2014).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , HutsonTE, CellaDet al. Pazopanib versus sunitinib in metastatic renal-cell carcinoma. N. Engl. J. Med.369(8), 722–731 (2013).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , HutsonTE, OlsenMRet al. Randomized Phase II trial of sunitinib on an intermittent versus continuous dosing schedule as first-line therapy for advanced renal cell carcinoma. J. Clin. Oncol.30(12), 1371–1377 (2012).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , HutsonTE, TomczakPet al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J. Clin. Oncol.27(22), 3584–3590 (2009).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , NosovD, EisenTet al. Tivozanib versus sorafenib as initial targeted therapy for patients with metastatic renal cell carcinoma: results from a Phase III trial. J. Clin. Oncol.31(30), 3791–3799 (2013).
   PubMed Web of Science ®Google Scholar
• Procopio G , VerzoniE, BracardaSet al. Overall survival for sorafenib plus interleukin-2 compared with sorafenib alone in metastatic renal cell carcinoma (mRCC): final results of the ROSORC trial. Ann. Oncol.24(12), 2967–2971 (2013).
   PubMed Web of Science ®Google Scholar
• Ravaud A , HawkinsR, GardnerJPet al. Lapatinib versus hormone therapy in patients with advanced renal cell carcinoma: a randomized Phase III clinical trial. J. Clin. Oncol.26(14), 2285–2291 (2008).
   PubMed Web of Science ®Google Scholar
• Rini BI , StenzlA, ZdrojowyRet al. IMA901, a multipeptide cancer vaccine, plus sunitinib versus sunitinib alone, as first-line therapy for advanced or metastatic renal cell carcinoma (IMPRINT): a multicentre, open-label, randomised, controlled, Phase III trial. Lancet Oncol.17(11), 1599–1611 (2016).
   PubMed Web of Science ®Google Scholar
• Rini BI , TomitaY, MelicharBet al. Overall survival analysis from a randomized Phase II study of axitinib with or without dose titration in first-line metastatic renal cell carcinoma. Clin. Genitourin. Cancer14(6), 499–503 (2016).
   PubMed Web of Science ®Google Scholar
• Procopio G , VerzoniE, BracardaSet al. Sorafenib with interleukin-2 vs sorafenib alone in metastatic renal cell carcinoma: the ROSORC trial. Br. J. Cancer104(8), 1256–1261 (2011).
   PubMed Web of Science ®Google Scholar
• Bamias A , KaradimouA, LampakiSet al. Prognostic stratification of patients with advanced renal cell carcinoma treated with sunitinib: comparison with the Memorial Sloan-Kettering prognostic factors model. BMC Cancer10, 45 (2010).
   PubMed Web of Science ®Google Scholar
• Day D , KanjanapanY, KwanEet al. Patterns of care for metastatic renal cell carcinoma in Australia. BJU Int.116(Suppl. 3), 36–41 (2015).
   PubMed Web of Science ®Google Scholar
• De Giorgi U , ScarpiE, SaccoCet al. Standard vs adapted sunitinib regimen in elderly patients with metastatic renal cell cancer: results from a large retrospective analysis. Clin. Genitourin. Cancer12(3), 182–189 (2014).
   PubMed Web of Science ®Google Scholar
• De Groot S , SleijferS, RedekopWKet al. Variation in use of targeted therapies for metastatic renal cell carcinoma: results from a Dutch population-based registry. BMC Cancer16, 364 (2016).
   PubMed Web of Science ®Google Scholar
• Heng DY , ChiKN, MurrayNet al. A population-based study evaluating the impact of sunitinib on overall survival in the treatment of patients with metastatic renal cell cancer. Cancer115(4), 776–783 (2009).
   PubMed Web of Science ®Google Scholar
• Joshi A , RamaswamyA, NoronhaVet al. Efficacy and safety of sorafenib in advanced renal cell cancer and validation of Heng criteria. Indian J. Cancer53(3), 423–428 (2016).
   PubMed Web of Science ®Google Scholar
• Kim MJ , ParkSH, LeeJL, LeeSH, LeeSJ, LimHY. A Korean multi-center, real-world, retrospective study of first-line pazopanib in unselected patients with metastatic renal clear-cell carcinoma. BMC Urol.16(1), 46 (2016).
   PubMedGoogle Scholar
• Kim SH , KimS, NamBHet al. Efficacy and safety of sorafenib therapy on metastatic renal cell carcinoma in Korean patients: results from a retrospective multicenter study. PLoS ONE10(8), e0135165 (2015).
   PubMed Web of Science ®Google Scholar
• Lalani AA , LiH, HengDYCet al. First-line sunitinib or pazopanib in metastatic renal cell carcinoma: the Canadian experience. Can. Urol. Assoc. J.11(3-4), 112–117 (2017).
   PubMed Web of Science ®Google Scholar
• Maroun R , FleuryL, NachbaurG, MaunouryF, VanhilleJL, Durand-ZaleskiI. Real-world costs and outcomes in metastatic renal cell carcinoma patients treated with targeted therapies: a cohort study from the French health insurance database. Curr. Med. Res. Opin.33(10), 1755–1762 (2017).
   PubMed Web of Science ®Google Scholar
• Matrana MR , BathalaT, CampbellMTet al. Outcomes of unselected patients with metastatic clear-cell renal cell carcinoma treated with first-line pazopanib therapy followed by vascular endothelial growth factor receptor tyrosine kinase inhibitors or mammalian target of rapamycin inhibitors: a single institution experience. BJU Int.118(2), 264–271 (2016).
   PubMed Web of Science ®Google Scholar
• Miyake H , MiyazakiA, HaradaK, FujisawaM. Assessment of efficacy, safety and quality of life of 110 patients treated with sunitinib as first-line therapy for metastatic renal cell carcinoma: experience in real-world clinical practice in Japan. Med. Oncol.31(6), 978 (2014).
   PubMed Web of Science ®Google Scholar
• Noize P , GrelaudA, BayJOet al. Real-life patterns of use, safety and effectiveness of sunitinib in first-line therapy of metastatic renal cell carcinoma: the SANTORIN cohort study. Pharmacoepidemiol. Drug Saf.26(12), 1561–1569 (2017).
   PubMed Web of Science ®Google Scholar
• Pan X , HuangH, HuangYet al. Sunitinib dosing schedule 2/1 improves tolerability, efficacy, and health-related quality of life in Chinese patients with metastatic renal cell carcinoma. Urol. Oncol.33(6), 268 (2015). e269-215
   Web of Science ®Google Scholar
• Perez-Valderrama B , ArranzArija JA, RodriguezSanchez Aet al. Validation of the International Metastatic Renal-Cell Carcinoma Database Consortium (IMDC) prognostic model for first-line pazopanib in metastatic renal carcinoma: the Spanish Oncologic Genitourinary Group (SOGUG) SPAZO study. Ann. Oncol.27(4), 706–711 (2016).
   PubMed Web of Science ®Google Scholar
• Poprach A , LakomyR, BortlicekZet al. Efficacy of sunitinib in elderly patients with metastatic renal cell carcinoma: data from real-world clinical practice. Drugs Aging33(9), 655–663 (2016).
   PubMed Web of Science ®Google Scholar
• Schnadig ID , HutsonTE, ChungHet al. Dosing patterns, toxicity, and outcomes in patients treated with first-line sunitinib for advanced renal cell carcinoma in community-based practices. Clin. Genitourin. Cancer12(6), 413–421 (2014).
   PubMed Web of Science ®Google Scholar
• Sheng X , ChiZ, CuiCet al. Efficacy and safety of sorafenib versus sunitinib as first-line treatment in patients with metastatic renal cell carcinoma: largest single-center retrospective analysis. Oncotarget7(19), 27044–27054 (2016).
   PubMedGoogle Scholar
• Tan HS , LiH, HongYWet al. Efficacy and safety of an attenuated-dose sunitinib regimen in metastatic renal cell carcinoma: results from a prospective registry in Singapore. Clin. Genitourin. Cancer13(4), e285–e295 (2015).
   PubMed Web of Science ®Google Scholar
• Vogelzang NJ , HackshawMD, HutsonTEet al. First-line and sequential use of pazopanib followed by mammalian target of rapamycin inhibitor therapy among patients with advanced renal cell carcinoma in a US community oncology setting. Clin. Genitourin. Cancer13(3), 210–217 (2015).
   PubMed Web of Science ®Google Scholar
• Zhang HL , QinXJ, WangHKet al. Clinicopathological and prognostic factors for long-term survival in Chinese patients with metastatic renal cell carcinoma treated with sorafenib: a single-center retrospective study. Oncotarget6(34), 36870–36883 (2015).
   PubMedGoogle Scholar
• Zhang HL , ShengXN, LiXSet al. Sorafenib versus sunitinib as first-line treatment agents in Chinese patients with metastatic renal cell carcinoma: the largest multicenter retrospective analysis of survival and prognostic factors. BMC Cancer17(1), 16 (2017).
   PubMedGoogle Scholar
• Dekkers OM , von ElmE, AlgraA, RomijnJA, VandenbrouckeJP. How to assess the external validity of therapeutic trials: a conceptual approach. Int. J. Epidemiol.39(1), 89–94 (2010).
   PubMed Web of Science ®Google Scholar
• Wagstaff J , JonesR, HawkinsRet al. Treatment patterns and clinical outcomes in patients with renal cell carcinoma in the UK: insights from the RECCORD registry. Ann. Oncol.27(1), 159–165 (2016).
   PubMed Web of Science ®Google Scholar
• Mitchell AP , HarrisonMR, WalkerMS, GeorgeDJ, AbernethyAP, HirschBR. Clinical trial participants with metastatic renal cell carcinoma differ from patients treated in real-world practice. J. Oncol. Pract.11(6), 491–497 (2015).
   PubMed Web of Science ®Google Scholar
• Harrison MR , HirschBR, GeorgeDJet al. Real-world outcomes in metastatic renal cell carcinoma: insights from a Joint Community-Academic Registry. J. Oncol. Pract.10(2), e63–72 (2014).
   PubMedGoogle Scholar
• Ruiz-Morales JM , SwierkowskiM, WellsJCet al. First-line sunitinib versus pazopanib in metastatic renal cell carcinoma: results from the International Metastatic Renal Cell Carcinoma Database Consortium. Eur. J. Cancer65, 102–108 (2016).
   PubMed Web of Science ®Google Scholar
• Heng DY , ChoueiriTK, RiniBIet al. Outcomes of patients with metastatic renal cell carcinoma that do not meet eligibility criteria for clinical trials. Ann. Oncol.25(1), 149–154 (2014).
   PubMed Web of Science ®Google Scholar
• Nieder C , SyedMA, DalhaugA, PawinskiA, NorumJ. Eligibility for Phase III clinical trials of systemic therapy in real-world patients with metastatic renal cell cancer managed in a rural region. Med. Oncol.34(9), 149 (2017).
   PubMed Web of Science ®Google Scholar
• Marschner N , StaehlerM, MullerLet al. Survival of patients with advanced or metastatic renal cell carcinoma in routine practice differs from that in clinical trials-analyses from the German Clinical RCC Registry. Clin. Genitourin. Cancer15(2), e209–e215 (2017).
   PubMedGoogle Scholar
• Gore ME , SzczylikC, PortaCet al. Final results from the large sunitinib global expanded-access trial in metastatic renal cell carcinoma. Br. J. Cancer113(1), 12–19 (2015).
   PubMed Web of Science ®Google Scholar
• Ramamoorthy A , KnepperTC, MerendaCet al. Demographic composition of select oncologic new molecular entities approved by the FDA between 2008 and 2017. Clin. Pharmacol. Ther.104(5), 940–948 (2018).
   PubMed Web of Science ®Google Scholar
• Stafford HS , SaltzsteinSL, ShimasakiS, SandersC, DownsTM, SadlerGR. Racial/ethnic and gender disparities in renal cell carcinoma incidence and survival. J. Urol.179(5), 1704–1708 (2008).
   PubMed Web of Science ®Google Scholar
• Jung EJ , LeeHJ, KwakC, KuJH, MoonKC. Young age is independent prognostic factor for cancer-specific survival of low-stage clear cell renal cell carcinoma. Urology73(1), 137–141 (2009).
   PubMed Web of Science ®Google Scholar
• Li P , WongYN, ArmstrongKet al. Survival among patients with advanced renal cell carcinoma in the pretargeted versus targeted therapy eras. Cancer Med.5(2), 169–181 (2016).
   PubMed Web of Science ®Google Scholar
• De Groot S , BlommesteinHM, RedekopWKet al. Potential health gains for patients with metastatic renal cell carcinoma in daily clinical practice: a real-world cost-effectiveness analysis of sequential first- and second-line treatments. PLoS ONE12(5), e0177364 (2017).
   PubMed Web of Science ®Google Scholar
• Motzer RJ , PenkovK, HaanenJet al. Avelumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N. Engl. J. Med.380, 1103–1115 (2019).
   PubMed Web of Science ®Google Scholar
• Rini BI , PlimackER, StusVet al. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N. Engl. J. Med.380, 1116–1127 (2019).
   PubMed Web of Science ®Google Scholar
• Fife KCJ , NolascoS, MatakidouA, WelshS, EisenT. Metastatic renal cancer: how many patients are we treating? . Presented at: National Cancer Research Institute Cancer Conference. 4–6 November, Glasgow, UK.
   Google Scholar
• Goebell PJ , StaehlerM, MullerLet al. Changes in treatment reality and survival of patients with advanced clear cell renal cell carcinoma - analyses from the German clinical RCC-registry. Clin. Genitourin. Cancer16(6), e1101–e1115 (2018).
   PubMed Web of Science ®Google Scholar
• Hirsch BR , BurkeJM, AgrawalMet al. Sequential therapy in metastatic renal cell carcinoma. J. Kidney Cancer VHL3(1), 23–35 (2016).
   PubMedGoogle Scholar
• Oyinlola JO , CampbellJ, KousoulisAA. Is real world evidence influencing practice? A systematic review of CPRD research in NICE guidances. BMC Health Serv. Res.16, 299 (2016).
   PubMed Web of Science ®Google Scholar
• Skovlund E , LeufkensHGM, SmythJF. The use of real-world data in cancer drug development. Eur. J. Cancer101, 69–76 (2018).
   PubMed Web of Science ®Google Scholar
• Benchimol EI , SmeethL, GuttmannAet al. The REporting of studies Conducted using Observational Routinely-collected health Data (RECORD) statement. PLoS Med.12(10), e1001885 (2015).
   PubMed Web of Science ®Google Scholar
• von Elm E , AltmanDG, EggerMet al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet370(9596), 1453–1457 (2007).
   PubMed Web of Science ®Google Scholar
• Hemkens LG , BenchimolEI, LanganSMet al. The reporting of studies using routinely collected health data was often insufficient. J. Clin. Epidemiol.79, 104–111 (2016).
   PubMed Web of Science ®Google Scholar
• US FDA . Cancer clinical trial eligibility criteria: minimum age for pediatric patients(2019). https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cancer-clinical-trial-eligibility-criteria-minimum-age-pediatric-patients
   Google Scholar
• US FDA . Cancer clinical trial eligibility criteria: patients with organ dysfunction or prior or concurrent malignancies (2019). https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cancer-clinical-trial-eligibility-criteria-patients-organ-dysfunction-or-prior-or-concurrent
   Google Scholar
• US FDA . Cancer clinical trial eligibility criteria: brain metastases (2019). https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cancer-clinical-trial-eligibility-criteria-brain-metastases
   Google Scholar
• US FDA . Cancer clinical trial eligibility criteria: patients with HIV, hepatitis B virus, or hepatitis C virus infections (2019). https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cancer-clinical-trial-eligibility-criteria-patients-hiv-hepatitis-b-virus-or-hepatitis-c-virus
   Google Scholar