Real-world comparison of healthcare resource utilization and costs of [¹⁷⁷Lu]Lu-DOTA-TATE in patients with progressive neuroendocrine tumors in England: a matched cohort analysis using data from the hospital episode statistics dataset

References

• Popa O, Taban SM, Pantea S, et al. The new WHO classification of gastrointestinal neuroendocrine tumors and immunohistochemical expression of somatostatin receptor 2 and 5. Exp Ther Med. 2021;22(4):1179–1187.
   PubMed Web of Science ®Google Scholar
• Oronsky B, Ma PC, Morgensztern D, et al. Nothing but NET: a review of neuroendocrine tumors and carcinomas. Neoplasia. 2017;19(12):991–1002.
   PubMed Web of Science ®Google Scholar
• Öberg K. Medical therapy of gastrointestinal neuroendocrine tumors. Visc Med. 2017;33(5):352–356.
   PubMed Web of Science ®Google Scholar
• Dasari A, Shen C, Halperin D, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–1342.
   PubMed Web of Science ®Google Scholar
• Genus TSE, Bouvier C, Wong KF, et al. Impact of neuroendocrine morphology on cancer outcomes and stage at diagnosis: a UK nationwide cohort study 2013-2015. Br J Cancer. 2019;121(11):966–972.
   PubMed Web of Science ®Google Scholar
• Genus T, Bouvier C, Wong K, et al. Incidence and prevalence of neuroendocrine tumours in England. UKI NETS 15th National Conference, London, UK, endocrine abstracts; 2017.
   Google Scholar
• van der Zwan JM, Trama A, Otter R, RARECARE WG, et al. Rare neuroendocrine tumours: results of the surveillance of rare cancers in Europe project. Eur J Cancer. 2013;49(11):2565–2578.
   PubMed Web of Science ®Google Scholar
• Fraenkel M, Kim M, Faggiano A, Knowledge NETwork, et al. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153–R163.
   PubMed Web of Science ®Google Scholar
• White BE, Bouvier C, Genus T, et al. O42 incidence of neuroendocrine neoplasms in England 2015–2017. Gut. 2021;70(Suppl 1):A23.
   Google Scholar
• Fitzgerald TL, Dennis SO, Kachare SD, et al. Increasing incidence of duodenal neuroendocrine tumors: Incidental discovery of indolent disease? Surgery. 2015;158(2):466–471.
   PubMed Web of Science ®Google Scholar
• Panzuto F, Merola E, Pavel ME, et al. Stage IV gastro‐entero‐pancreatic neuroendocrine neoplasms: a risk score to predict clinical outcome. The Oncologist. 2017;22(4):409–415.
   PubMed Web of Science ®Google Scholar
• Klimstra DS, Modlin IR, Coppola D, et al. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas. 2010;39(6):707–712.
   PubMed Web of Science ®Google Scholar
• Klöppel G. Classification and pathology of gastroenteropancreatic neuroendocrine neoplasms. Endocr Relat Cancer. 2011;18(S1):S1–S16.
   PubMed Web of Science ®Google Scholar
• Strosberg J, Nasir A, Coppola D, et al. Correlation between grade and prognosis in metastatic gastroenteropancreatic neuroendocrine tumors. Hum Pathol. 2009;40(9):1262–1268.
   PubMed Web of Science ®Google Scholar
• Cives M, Strosberg J. An update on gastroenteropancreatic neuroendocrine tumors. Oncology. 2014;28(9):749–756.
   PubMed Web of Science ®Google Scholar
• Man D, Wu J, Shen Z, et al. Prognosis of patients with neuroendocrine tumor: a SEER database analysis. Cancer Manag Res. 2018;10:5629–5638.
   PubMed Web of Science ®Google Scholar
• Pavel M, Öberg K, Falconi M, et al. Gastroenteropancreatic neuroendocrine neoplasms: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(5):844–860.
   PubMed Web of Science ®Google Scholar
• National Comprehensive Cancer Network. NCCN guidelines version 1.2021 neuroendocrine and adrenal tumors; 2021. Available from: https://www.nccn.org/professionals/physician_gls/pdf/neuroendocrine.pdf
   Google Scholar
• Rinke A, Müller HH, Schade-Brittinger C, PROMID Study Group, et al. Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID study group. J Clin Oncol. 2009;27(28):4656–4663.
   PubMed Web of Science ®Google Scholar
• Caplin ME, Pavel M, Ćwikła JB, CLARINET Investigators, et al. Anti-tumour effects of lanreotide for pancreatic and intestinal neuroendocrine tumours: the CLARINET open-label extension study. Endocr Relat Cancer. 2016;23(3):191–199.
   PubMed Web of Science ®Google Scholar
• Caplin ME, Pavel M, Ćwikła JB, et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371(3):224–233.
   PubMed Web of Science ®Google Scholar
• Jalbert JJ, Casciano R, Meng J, et al. Treatment patterns and health resource use among patients with metastatic gastroenteropancreatic neuroendocrine tumors treated at a tertiary referral center. Oncologist. 2020;25(4):e644–e650.
   PubMed Web of Science ®Google Scholar
• Palazzo M, Lombard-Bohas C, Cadiot G, et al. Ki67 proliferation index, hepatic tumor load, and pretreatment tumor growth predict the antitumoral efficacy of lanreotide in patients with malignant digestive neuroendocrine tumors. Eur J Gastroenterol Hepatol. 2013;25(2):232–238.
   PubMed Web of Science ®Google Scholar
• Pavel M, Ćwikła JB, Lombard-Bohas C, et al. Efficacy and safety of high-dose lanreotide autogel in patients with progressive pancreatic or midgut neuroendocrine tumours: CLARINET FORTE phase 2 study results. Eur J Cancer. 2021;157:403–414.
   PubMed Web of Science ®Google Scholar
• Raymond E, Dahan L, Raoul J-L, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med. 2011;364(6):501–513.
   PubMed Web of Science ®Google Scholar
• Yao JC, Fazio N, Singh S, et al. Everolimus for the treatment of advanced, non-functional neuroendocrine tumours of the lung or gastrointestinal tract (RADIANT-4): a randomised, placebo-controlled, phase 3 study. Lancet. 2016;387(10022):968–977.
   PubMed Web of Science ®Google Scholar
• Yao JC, Shah MH, Ito T, et al. Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med. 2011;364(6):514–523.
   PubMed Web of Science ®Google Scholar
• Strosberg JR, Caplin ME, Kunz PL, NETTER-1 investigators, et al. 177Lu-Dotatate plus long-acting octreotide versus high‑dose long-acting octreotide in patients with midgut neuroendocrine tumours (NETTER-1): final overall survival and long-term safety results from an open-label, randomised, controlled, phase 3 trial. Lancet Oncol. 2021;22(12):1752–1763.
   PubMed Web of Science ®Google Scholar
• Strosberg J, El-Haddad G, Wolin E, et al. Phase 3 trial of 177Lu-Dotatate for midgut neuroendocrine tumors. N Engl J Med. 2017;376(2):125–135.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. Lutathera product information – Annex I summary of product characteristics; 2018 [cited 2021 Mar 17]. Available from: https://www.ema.europa.eu/en/documents/product-information/lutathera-epar-product-information_en.pdf.
   Google Scholar
• U.S Food & Drug Administration. FDA approves lutetium Lu 177 dotatate for treatment of GEP-NETS; 2018 [cited 2021 Jul 19]. Available from: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-lutetium-lu-177-dotatate-treatment-gep-nets.
   Google Scholar
• Brabander T, van der Zwan WA, Teunissen JJM, et al. Long-term efficacy, survival, and safety of [177Lu-DOTA0,Tyr3]octreotate in patients with gastroenteropancreatic and bronchial neuroendocrine tumors. Clin Cancer Res. 2017;23(16):4617–4624.
   PubMed Web of Science ®Google Scholar
• National Institute for Health and Care Excellence. Lutetium (177Lu) oxodotreotide for treating unresectable or metastatic treating unresectable or metastatic neuroendocrine tumours neuroendocrine tumour – technology appraisal guidance [TA539]; 2018 [cited 2021 Jul 6]. Available from: https://www.nice.org.uk/guidance/ta539/resources/lutetium-177lu-oxodotreotide-for-treating-unresectable-or-metastatic-neuroendocrine-tumours-pdf-82606909338565.
   Google Scholar
• Scottish Medicine Consortium. Lutetium (177Lu) oxodotreotide 370MBq/mL solution for infusion (Lutathera) SMC No 1337/18: Scottish Medicine Consortium; 2018 [cited 2021 July 6]. Available from: https://www.scottishmedicines.org.uk/media/3557/lutetium-177lu-oxodotreotide-lutathera-final-june-2018-for-website.pdf.
   Google Scholar
• Smith-Palmer J, Leeuwenkamp OR, Virk J, et al. Lutetium oxodotreotide (177Lu-Dotatate) for the treatment of unresectable or metastatic progressive gastroenteropancreatic neuroendocrine tumors: a cost-effectiveness analysis for Scotland. BMC Cancer. 2021;21(1):10.
   PubMed Web of Science ®Google Scholar
• Palmer J, Leeuwenkamp O. Cost-effectiveness of lutetium (177Lu) oxodotreotide vs everolimus in gastroenteropancreatic neuroendocrine tumors in Norway and Sweden. World J Clin Cases. 2020;8(20):4793–4806.
   PubMed Web of Science ®Google Scholar
• Leeuwenkamp O, Smith-Palmer J, Ortiz R, et al. Cost-effectiveness of lutetium [177Lu] oxodotreotide versus best supportive care with octreotide in patients with midgut neuroendocrine tumors in France. J Med Econ. 2020;23(12):1534–1541.
   PubMed Web of Science ®Google Scholar
• Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228–247.
   PubMed Web of Science ®Google Scholar
• Boyd A, Cornish R, Johnson L, et al. Understanding hospital episode statistics (HES) London, UK: CLOSER; 2017 [cited 2021 Mar 18]. Available from: https://www.closer.ac.uk/wp-content/uploads/CLOSER-resource-understanding-hospital-episode-statistics-2018.pdf.
   Google Scholar
• Rosenbaum PR, Rubin DB. The central role of the propensity score in observational studies for causal effects. Biometrika. 1983;70(1):41–55.
   Web of Science ®Google Scholar
• Caliendo M, Kopeinig S. Some practical guidance for the implementation of propensity score matching. J Economic Surveys. 2008;22(1):31–72.
   Web of Science ®Google Scholar
• Austin PC. Some methods of propensity-score matching had superior performance to others: results of an empirical investigation and Monte Carlo simulations. Biom J. 2009;51(1):171–184.
   PubMed Web of Science ®Google Scholar
• Becker SO, Ichino A. Estimation of average treatment effects based on propensity scores. The Stata Journal. 2002;2(4):358–377.
   Web of Science ®Google Scholar
• Austin PC. The relative ability of different propensity score methods to balance measured covariates between treated and untreated subjects in observational studies. Med Decis Making. 2009;29(6):661–677.
   PubMed Web of Science ®Google Scholar
• Rubin DB. Using propensity scores to help design observational studies: application to the tobacco litigation. Health Serv Outcomes Res Methodol. 2001;2(3/4):169–188.
   Google Scholar
• National Health Services. NHS data model and dictionary – care professional out-patient attendance; 2021 [cited 2021 Sept 15]. Available from: https://datadictionary.nhs.uk/nhs_business_definitions/care_professional_out-patient_attendance.html.
   Google Scholar
• National Health Services. NHS data model and dictionary – patient classification; 2021 [cited 2021 Sep 15]. Available from: https://datadictionary.nhs.uk/attributes/patient_classification.html.
   Google Scholar
• European Medicines Agency. Afinitor product information – Annex I summary of product characteristics; 2021 [cited 2021 Mar 17]. Available from: https://www.ema.europa.eu/en/documents/product-information/afinitor-epar-product-information_en.pdf.
   Google Scholar
• European Medicines Agency. Sutent product information – Annex I summary of product characteristics; 2019 [cited 2021 Mar 17]. Available from: https://www.ema.europa.eu/en/documents/product-information/sutent-epar-product-information_en.pdf.
   Google Scholar
• Strosberg J, Casciano R, Stern L, et al. United States-based practice patterns and resource utilization in advanced neuroendocrine tumor treatment. World J Gastroenterol. 2013;19(15):2348–2354.
   PubMed Web of Science ®Google Scholar
• Clement D, Navalkissoor S, Srirajaskanthan R, et al. Efficacy and safety of 177Lu‑DOTATATE in patients (pts) with advanced pancreatic neuroendocrine tumors (pNETs): data from the NETTER-R international, retrospective registry. Eur J Nucl Med Mol Imaging. 2022. DOI:https://doi.org/10.1007/s00259-022-05771-3.
   Google Scholar
• Strosberg J, Wolin E, Chasen B, NETTER-1 Study Group, et al. Health-related quality of life in patients with progressive midgut neuroendocrine tumors treated with 177Lu-Dotatate in the phase III NETTER-1 trial. J Clin Oncol. 2018;36(25):2578–2584.
   PubMed Web of Science ®Google Scholar
• Spada F, Campana D, Lamberti G, et al. [177Lu]Lu-DOTA-TATE versus standard of care in adult patients with gastro-enteropancreatic neuroendocrine tumours (GEP-NETs): a cost-consequence analysis from an Italian hospital perspective. Eur J Nucl Med Mol Imaging. 2022;49(6):2037–2048.
   PubMed Web of Science ®Google Scholar