Feasibility and early clinical impact of precision medicine for late-stage cancer patients in a regional public academic hospital

References

• Kamps R, Brandão R, Bosch B, et al. Next-Generation sequencing in oncology: genetic diagnosis, risk prediction and cancer classification. Int J Mol Sci. 2017;18(2):308.
   PubMed Web of Science ®Google Scholar
• Yates LR, Seoane J, Le Tourneau C, et al. The european society for medical oncology (ESMO) precision medicine glossary. Ann Oncol. 2018;29(1):30–35.
   PubMed Web of Science ®Google Scholar
• Morganti S, Tarantino P, Ferraro E, et al. Next generation sequencing (NGS): a revolutionary technology in pharmacogenomics and personalized medicine in cancer. Adv Exp Med Biol. 2019;1168:9–30.
   Google Scholar
• Malone ER, Oliva M, Sabatini PJB, et al. Molecular profiling for precision cancer therapies. Genome Med. 2020;12(1):8.
   PubMed Web of Science ®Google Scholar
• Berger MF, Mardis ER. The emerging clinical relevance of genomics in cancer medicine. Nat Rev Clin Oncol. 2018;15(6):353–365.
   PubMed Web of Science ®Google Scholar
• Duke ES, J. Fusco M, DeMoss P, et al. Highlights of FDA oncology approvals in 2022: tissue-agnostic indications, dosage optimization, and diversity in drug development. Cancer Discov. 2022;12(12):2739–2746.
   PubMed Web of Science ®Google Scholar
• Prahallad A, Sun C, Huang S, et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature. 2012;483(7387):100–103.
   PubMed Web of Science ®Google Scholar
• van der Velden DL, Hoes LR, van der Wijngaart H, et al. The drug rediscovery protocol facilitates the expanded use of existing anticancer drugs. Nature. 2019;574(7776):127–131.
   PubMed Web of Science ®Google Scholar
• Schwaederle M, Zhao M, Lee JJ, et al. Impact of precision medicine in diverse cancers: a meta-analysis of phase II clinical trials. J Clin Oncol. 2015;33(32):3817–3825.
   PubMed Web of Science ®Google Scholar
• Wheeler DA, Takebe N, Hinoue T, et al. Molecular features of cancers exhibiting exceptional responses to treatment. Cancer Cell. 2021;39(1):38.e7–53.e7.
   Web of Science ®Google Scholar
• Sharma MB, Carus A, Sunde L, et al. BRCA-associated pancreatico-biliary neoplasms: four cases illustrating the emerging clinical impact of genotyping. Acta Oncol. 2016;55(3):377–381.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Fu Q, Bai X, et al. Molecular profiling–based precision medicine in cancer: a review of current evidence and challenges. Front Oncol. 2020;10:532403.
   PubMed Web of Science ®Google Scholar
• Le Tourneau C, Delord J-P, Gonçalves A, et al. Molecularly targeted therapy based on tumour molecular profiling versus conventional therapy for advanced cancer (SHIVA): a multicentre, open-label, proof-of-concept, randomised, controlled phase 2 trial. Lancet Oncol. 2015;16(13):1324–1334.
   PubMed Web of Science ®Google Scholar
• Miller RW, Hutchcraft ML, Weiss HL, et al. Molecular tumor board–assisted care in an advanced cancer population: results of a phase II clinical trial. JCO Precis Oncol. 2022;(6):e2100524.
   PubMedGoogle Scholar
• Von Hoff DD, Stephenson JJ, Rosen P, et al. Pilot study using molecular profiling of patients’ tumors to find potential targets and select treatments for their refractory cancers. J Clin Oncol. 2010;28(33):4877–4883.
   PubMed Web of Science ®Google Scholar
• Zimmer K, Kocher F, Spizzo G, et al. Treatment according to molecular profiling in relapsed/refractory cancer patients: a review focusing on latest profiling studies. Comput Struct Biotechnol J. 2019;17:447–453.
   PubMed Web of Science ®Google Scholar
• Tsimberidou AM, Eggermont AMM, Schilsky RL. Precision cancer medicine: the future Is now, only better. Am Soc Clin Oncol Educ Book. 2014;(34):61–69.
   PubMedGoogle Scholar
• Nakamura Y, Fujisawa T, Taniguchi H, et al. SCRUM‐Japan GI‐SCREEN and MONSTAR‐SCREEN: path to the realization of biomarker‐guided precision oncology in advanced solid tumors. Cancer Sci. 2021;112(11):4425–4432.
   PubMed Web of Science ®Google Scholar
• Meric-Bernstam F, Farhangfar C, Mendelsohn J, et al. Building a personalized medicine infrastructure at a major cancer center. J Clin Oncol. 2013;31(15):1849–1857.
   PubMed Web of Science ®Google Scholar
• American Association for Cancer Research. Bringing precision medicine to community oncologists. Cancer Discov. 2017;7(1):6–7.
   Google Scholar
• Ladekarl M, Rasmussen LS, Kirkegård J, et al. Disparity in use of modern combination chemotherapy associated with facility type influences survival of 2655 patients with advanced pancreatic cancer. Acta Oncol. 2022;61(3):277–285.
   PubMed Web of Science ®Google Scholar
• Bruno DS, Hess LM, Li X, et al. Disparities in biomarker testing and clinical trial enrollment among patients with lung, breast, or colorectal cancers in the United States. JCO Precis Oncol. 2022;6:e2100427.
   PubMed Web of Science ®Google Scholar
• Danmarks Statistik. Befolkningstal. 2022. Available from: https://www.dst.dk/da/Statistik/emner/borgere/befolkning/befolkningstal
   Google Scholar
• Finan C, Gaulton A, Kruger FA, et al. The druggable genome and support for target identification and validation in drug development. Sci Transl Med. 2017;9(383):eaag1166.
   PubMed Web of Science ®Google Scholar
• Harris PA, Taylor R, Thielke R, et al. Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–381.
   PubMed Web of Science ®Google Scholar
• Johnson NT, Dhroso A, Hughes KJ, et al. Biological classification with RNA-seq data: can alternatively spliced transcript expression enhance machine learning classifiers? RNA. 2018;24(9):1119–1132.
   PubMed Web of Science ®Google Scholar
• Bødker JS, Sønderkær M, Vesteghem C, et al. Development of a precision medicine workflow in hematological cancers, aalborg university hospital, Denmark. Cancers. 2020;12(2):312.
   PubMed Web of Science ®Google Scholar
• McKenna A, Hanna M, Banks E, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–1303.
   PubMed Web of Science ®Google Scholar
• QIAGEN. QIAGEN Digital Insights. Advancing molecular intelligence from bench to bedside. [cited 2023 Jan 1]. Available from: https://digitalinsights.qiagen.com/
   Google Scholar
• Li MM, Datto M, Duncavage EJ, et al. Standards and guidelines for the interpretation and reporting of sequence variants in cancer. J Mol Diagn. 2017;19(1):4–23.
   PubMed Web of Science ®Google Scholar
• Røe OD, Stella GM. Malignant pleural mesothelioma: history, controversy and future of a manmade epidemic. Eur Respir Rev. 2015;24(135):115–131.
   PubMed Web of Science ®Google Scholar
• Richards S, Aziz N, Bale S, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med. 2015;17(5):405–424.
   PubMed Web of Science ®Google Scholar
• Vesteghem C, Brøndum RF, Sønderkær M, et al. Implementing the FAIR data principles in precision oncology: review of supporting initiatives. Brief Bioinform. 2020;21(3):936–945.
   PubMed Web of Science ®Google Scholar
• Vesteghem C, Dahl S, Brøndum R, et al. Implementing a data infrastructure for precision oncology projects leveraging REDCap. medRxiv. 2022. DOI:10.1101/2022.05.09.22274599
   Google Scholar
• Kringelbach T, Højgaard M, Rohrberg K, et al. ProTarget: a danish nationwide clinical trial on targeted cancer treatment based on genomic profiling – a national, phase 2, prospective, multi-drug, non-randomized, open-label basket trial. BMC Cancer. 2023;23(1):182.
   PubMed Web of Science ®Google Scholar
• Yam C, Ma BBY, Yap TA. Global implementation of precision oncology. JCO Precis Oncol. 2021;(5):854–858.
   Google Scholar
• Owens J. Determining druggability. Nat Rev Drug Discov. 2007;6(3):187–187.
   Web of Science ®Google Scholar
• Perakis SO, Weber S, Zhou Q, et al. Comparison of three commercial decision support platforms for matching of next-generation sequencing results with therapies in patients with cancer. ESMO Open. 2020;5(5):e000872.
   PubMed Web of Science ®Google Scholar
• Koopman B, van der Wekken AJ, ter Elst A, et al. Relevance and effectiveness of molecular tumor board recommendations for patients with non–small-cell lung cancer with rare or complex mutational profiles. JCO Precis Oncol. 2020;4:393–410.
   PubMed Web of Science ®Google Scholar
• Condorelli R, Mosele F, Verret B, et al. Genomic alterations in breast cancer: level of evidence for actionability according to ESMO scale for clinical actionability of molecular targets (ESCAT). Ann Oncol. 2019;30(3):365–373.
   PubMed Web of Science ®Google Scholar
• Moreira A, Masliah-Planchon J, Callens C, et al. Efficacy of molecularly targeted agents given in the randomised trial SHIVA01 according to the ESMO scale for clinical actionability of molecular targets. Eur J Cancer. 2019;121:202–209.
   PubMed Web of Science ®Google Scholar
• Fairley JA, Deans ZC, Treacy RJL, et al. An independent assessment of a commercial clinical interpretation software indicates that software can mitigate variation in human assessment. J Mol Pathol. 2022;3(3):125–139.
   Google Scholar
• Tamborero D, Dienstmann R, Rachid MH, et al. The molecular tumor board portal supports clinical decisions and automated reporting for precision oncology. Nat Cancer. 2022;3(2):251–261.
   PubMedGoogle Scholar
• Katsoulakis E, Duffy JE, Hintze B, et al. Comparison of annotation services for next-generation sequencing in a large-scale precision oncology program. JCO Precis Oncol. 2020;(4):212–221.
   Google Scholar
• Molica S, Seymour JF, Polliack AA. Perspective on prognostic models in chronic lymphocytic leukemia in the era of targeted agents. Hematol Oncol. 2021;39(5):595–604.
   PubMed Web of Science ®Google Scholar
• Ortega-Martorell S, Riley P, Olier I, et al. Breast cancer patient characterisation and visualisation using deep learning and fisher information networks. Sci Rep. 2022;12(1):14004.
   PubMed Web of Science ®Google Scholar
• Koleva-Kolarova R, Buchanan J, Vellekoop H, et al. Financing and reimbursement models for personalised medicine: a systematic review to identify current models and future options. Appl Health Econ Health Policy. 2022;20(4):501–524.
   PubMed Web of Science ®Google Scholar
• Wercholuk AN, Parikh AA, Snyder RA. The road less traveled: transportation barriers to cancer care delivery in the rural patient population. JCO Oncol Pract. 2022;18(9):652–662.
   PubMedGoogle Scholar
• Lam M, Tran B, Beck S, et al. Precision oncology using a clinician-directed, tailored approach to molecular profiling. Asia Pac J Clin Oncol. 2018;14(1):84–90.
   PubMed Web of Science ®Google Scholar
• Ma BB, Hui EP, Mok TS. Population-based differences in treatment outcome following anticancer drug therapies. Lancet Oncol. 2010;11(1):75–84.
   PubMed Web of Science ®Google Scholar
• Andre F, Mardis E, Salm M, et al. Prioritizing targets for precision cancer medicine. Ann Oncol. 2014;25(12):2295–2303.
   PubMed Web of Science ®Google Scholar
• Aaltonen LA, Abascal F, Abeshouse A, et al. Pan-cancer analysis of whole genomes. Nature. 2020;578(7793):82–93.
   PubMed Web of Science ®Google Scholar
• Garraway LA, Verweij J, Ballman KV. Precision oncology: an overview. J Clin Oncol. 2013;31(15):1803–1805.
   PubMed Web of Science ®Google Scholar
• Sadik H, Pritchard D, Keeling D-M, et al. Impact of clinical practice gaps on the implementation of personalized medicine in advanced non–small-cell lung cancer. JCO Precis Oncol. 2022;6:e2200246.
   PubMed Web of Science ®Google Scholar
• Réda M, Richard C, Bertaut A, et al. Implementation and use of whole exome sequencing for metastatic solid cancer. EBioMedicine. 2020;51:102624.
   PubMed Web of Science ®Google Scholar
• Bayle A, Peyraud F, Belcaid L, et al. Liquid versus tissue biopsy for detecting actionable alterations according to the ESMO scale for clinical actionability of molecular targets in patients with advanced cancer: a study from the french national center for precision medicine (PRISM). Ann Oncol. 2022;33(12):1328–1331.
   PubMed Web of Science ®Google Scholar
• Dupain C, Masliah‐Planchon J, Gu C, et al. Fine‐needle aspiration as an alternative to core needle biopsy for tumour molecular profiling in precision oncology: prospective comparative study of next‐generation sequencing in cancer patients included in the SHIVA02 trial. Mol Oncol. 2021;15(1):104–115.
   PubMed Web of Science ®Google Scholar
• Cheng F, Su L, Qian C. Circulating tumor DNA: a promising biomarker in the liquid biopsy of cancer. Oncotarget. 2016;7(30):48832–48841.
   PubMedGoogle Scholar
• Topham JT, O’Callaghan CJ, Feilotter H, et al. Circulating tumor DNA identifies diverse landscape of acquired resistance to anti–epidermal growth factor receptor therapy in metastatic colorectal cancer. J Clin Oncol. 2023;41(3):485–496.
   PubMed Web of Science ®Google Scholar
• Chan HT, Chin YM, Low S-K. Circulating tumor DNA-Based genomic profiling assays in adult solid tumors for precision oncology: recent advancements and future challenges. Cancers. 2022;14(13):3275.
   PubMed Web of Science ®Google Scholar
• van de Haar J, Hoes LR, Roepman P, et al. Limited evolution of the actionable metastatic cancer genome under therapeutic pressure. Nat Med. 2021;27(9):1553–1563.
   PubMed Web of Science ®Google Scholar
• Vesteghem C, Brøndum RF, Mouritzen MT, et al. Thirty-day mortality following systemic anticancer therapy: evaluating risk factors without selection bias in a real-world, population-based cohort from 2009 to 2019. Clin Oncol. 2022;34(8):487–496.
   Web of Science ®Google Scholar
• Tuxen IV, Rohrberg KS, Oestrup O, et al. Copenhagen prospective personalized oncology (CoPPO)—clinical utility of using molecular profiling to select patients to phase I trials. Clin Cancer Res. 2019;25(4):1239–1247.
   PubMed Web of Science ®Google Scholar
• Plana D, Palmer AC, Sorger PK. Independent drug action in combination therapy: implications for precision oncology. Cancer Discov. 2022;12(3):606–624.
   PubMed Web of Science ®Google Scholar
• Olivier M, Asmis R, Hawkins GA, et al. The need for multi-omics biomarker signatures in precision medicine. Int J Mol Sci. 2019;20(19):4781.
   PubMed Web of Science ®Google Scholar
• Veal GJ, Amankwatia EB, Paludetto M-N, et al. Pharmacodynamic therapeutic drug monitoring for cancer: challenges, advances, and future opportunities. Ther Drug Monit. 2019;41(2):142–159.
   PubMed Web of Science ®Google Scholar
• Bertelsen B, Tuxen IV, Yde CW, et al. High frequency of pathogenic germline variants within homologous recombination repair in patients with advanced cancer. NPJ Genom Med. 2019;4(1):13.
   PubMedGoogle Scholar
• Tsimberidou AM, Iskander NG, Hong DS, et al. Personalized medicine in a phase I clinical trials program: the MD anderson cancer center initiative. Clin Cancer Res. 2012;18(22):6373–6383.
   PubMed Web of Science ®Google Scholar