Can biosimilar products be interchangeable? Pharmaceutical perspective in the implementation of biosimilars in oncology

Ferreira PMP and Pessoa C. Molecular biology of human epidermal receptors, signaling pathways and targeted therapy against cancers: new evidences and old challenges. Braz J Pharm Sci 2017; 53: 1–17.

Hirata BKB Oda JMM Guembarovski RL , et al. Molecular markers for breast cancer: prediction on tumor behavior. Dis Markers 2014; 2014: 513158.

Wang J Xu B. Targeted therapeutic options and future perspectives for HER2-positive breast cancer. Signal Transduct Target Ther 2019; 4: 34.

Scavone C Rafaniello C Berrino L , et al. Strengths, weaknesses and future challenges of biosimilars ’ development. An opinion on how to improve the knowledge and use of biosimilars in clinical practice. Pharmacol Res 2017; 126: 138–142.

Tkaczuk KHR Jacobs IA. Biosimilars in oncology: from development to clinical practice. Semin Oncol 2014; 41: S3–S12.

U.S. Food and Drug Administration - FDA. Biosimilar and Interchangeable Products. FDA, www.fda.gov/drugs/biosimilars/biosimilar-and-interchangeable-products#. :∼:text=A biosimilar is a biological,existing FDA-approved reference product. Published 2017. (accessed 16 April 2021).

Bui LA Taylor C. Developing clinical trials for biosimilars. Semin Oncol 2014; 41: S15–S25.

Henry D Taylor C. Pharmacoeconomics of cancer therapies: considerations with the introduction of biosimilars. Semin Oncol 2014; 41: S13–S20.

Ahmed I Kaspar B Sharma U. Biosimilars: impact of biologic product life cycle and European experience on the regulatory trajectory in the United States. Clin Ther 2012; 34: 400–419.

Klein AV Wang J Bedford P. Subsequent entry biologics (biosimilars) in Canada: approaches to interchangeability and the extrapolation of indications and uses. Generics Biosimilars Initiat J 2014; 3: 150–154.

USF. and DA. Biosimilars: questions and answers regarding implementation of the Biologic Price Competition and Innovation Act of 2009. Silver Spring, www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatory%0AInformation/Guidances/UCM444661.pdf (2015, accessed 23 November 2019).

Crespi-Lofton J Skelton JB. The growing role of biologics and biosimilars in the United States: perspectives from the APhA biologics and biosimilars stakeholder conference. J Am Pharm Assoc 2017; 57: e15–e27.

Chirino AJ Mire-Sluis A. Characterizing biological products and assessing comparability following manufacturing changes. Nat Biotechnol 2004; 22: 1383–1391.

Dudzinski DM Kesselheim AS. Scientific and legal viability of follow-on protein drugs. N Engl J Med 2008; 358: 843–849.

EMA. Biosimilar medicines. Did you know?, www.medicinesforeurope.com/biosimilar-medicines/did-you-know/ (2019, accessed 23 November 2019).

Santos S Lobo JMS Silva AC. Biosimilar medicines used for cancer therapy in Europe: a review. Drug Discov Today 2019; 24: 293–299.

U.S. FDA. Scientific considerations in demonstrating biosimilarity to a reference product. Guidance for industry. Silver Spring, www.fda.gov/ucm/groups/%0Afdagov-public/documents/document/ucm291128.pdf. (2015, accessed 23 November 2019).

Bennett CL Chen B Hermanson T , et al. Regulatory and clinical considerations for biosimilar oncology drugs. Lancet Oncol 2014; 15: e594–e605.

Kwon O Joung J Park Y , et al. Considerations of critical quality attributes in the analytical comparability assessment of biosimilar products. Biologicals 2017; 48: 101–108.

EMA. Guideline on similar biological medicinal products, www.ema.europa.eu/en/documents/scientific-guideline/guideline-similar-biological-medicinal-products-rev1_en.pdf (2014, accessed 24 November 2019).

WHO. Guidelines on evaluation of similar biotherapeutic products (SBPs). 2013. (977):51-89, www.who.int/biologicals/publications/trs/areas/biological_therapeutics/TRS_977_Annex_2.pdf?ua=1. (accessed 30 April 2021).

Weise M. From bioequivalence to biosimilars: how much do regulators dare? Z Evid Fortbild Qual Gesundhwes 2019; 140: 58–62.

Duivelshof BL Jiskoot W Beck A , et al. Glycosylation of biosimilars: recent advances in analytical characterization and clinical implications. Anal Chim Acta 2019; 1089: 1–18.

Higel F Seidl A Sörgel F , et al. N-glycosylation heterogeneity and the influence on structure, function and pharmacokinetics of monoclonal antibodies and Fc fusion proteins. Eur J Pharm Biopharm 2016; 100: 94–100.

Li W Yang B Zhou D , et al. Discovery and characterization of antibody variants using mass spectrometry-based comparative analysis for biosimilar candidates of monoclonal antibody drugs. J Chromatogr B 2016; 1025: 57–67.

ANVISA AN de VS-. Intercambialidade entre produtos registrados pela via de desenvolvimento por comparabilidade (“biossimilares”) e o produto biológico comparador. ANVISA, www.gov.br/anvisa/pt-br (2017, accessed 17 April 2021).

U.S. FDA. Food and drug administration. Considerations in demonstrating interchangeability with a reference product guidance for industry. Draft guidance. Silver Spring: Author. 2017.

O’Brien GL O’Mahony C Cooke K , et al. Cost minimization analysis of intravenous or subcutaneous trastuzumab treatment in patients with HER2-positive breast cancer in Ireland. Clin Breast Cancer 2019; 19: e440–e451.

Cuellar S McBride A Medina P. Pharmacist perspectives and considerations for implementation of therapeutic oncology biosimilars in practice. Am J Heal Pharm 2019; 76: 1725–1738.

Markus R Liu J Ramchandani M , et al. Developing the totality of evidence for biosimilars: regulatory considerations and building confidence for the healthcare community. BioDrugs 2017; 31: 175–187.

Lai Z Noce A. La. Key design considerations on comparative clinical efficacy studies for biosimilars: adalimumab as an example. Rheum Musculoskelet Dis 2016; 2: 1–13.

U.S. Food and Drug Administration – FDA. Scientific considerations in demonstrating biosimilarity to a reference product, www.fda.gov/media/82647/download (2015, accessed 30 April 2021).

U.S. Food and Drug Administration – FDA. BLA approval, www.accessdata.fda.gov/drugsatfda_docs/appletter/2015/125553Orig1s000ltr.pdf (2015, accessed 30 April 2021).

Anvisa A. d V. Resolução da diretoria colegiada – RDC n° 55, de 16 de dezembro de 2010. Ministério da Saúde, http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2010/res0055_16_12_2010.html#. :∼:text=Dispõe sobre o registro de,o inciso IV do art (2010, accessed 30 April 2021).

Weise M Kurki P Wolff-Holz E , et al. Biosimilars: the science of extrapolation. Blood 2014; 124: 3191–3196.

Braud EL Cross JD Davenport-Ennis N , et al. NCCN biosimilars white paper: regulatory, scientific, and patient safety perspectives. J Natl Compr Cancer Netw 2011; 9: S1–S22.

Whalen J. Recognizing and addressing challenges to the adoption of trastuzumab biosimilars and HER2-targeted therapies. Am J Manag Care 2020; 26: S23–S31.

Konstantinidou S Papaspiliou A Kokkotou E. Current and future roles of biosimilars in oncology practice. Oncol Lett 2020; 19: 45–51.

Saleem T, Qurashi H, Jamali M, et al. Biosimilars as a future, promising solution for financial toxicity: a review with emphasis on bevacizumab. Cureus 2020; 12: e9300.

Trapani D Curigliano G. How can biosimilars change the trajectory of breast cancer therapy? Expert review of anticancer therapy. Expert Rev Anticancer Ther 2020; 20: 325–328.

Waller CF and Friganovic A. Biosimilars in oncology: key role of nurses in patient education. Futur Oncol 2020; 16: 1931–1939.

Krendyukov A and Schiestl M. Biosimilars in oncology: a decade of experience with granulocyte colonystimulating factor and its implications for monoclonal antibodies. Crit Rev Oncol Hematol 2019; 23: 102785.

Aapro M Bokemeyer C Ludwig H , et al. Chemotherapy-induced (febrile) neutropenia prophylaxis with biosimilar filgrastim in elderly versus non-elderly cancer patients : Patterns, outcomes, and determinants (MONITOR-GCSF study). J Geriatr Oncol 2017; 8: 86–95.

Damaj GL Benbrahim O Hacini M , et al. ZOHé: a prospective study of the use of biosimilar filgrastim zarzio in clinical practice in patients treated with chemotherapy for lymphoid malignancies. Clin Lymphoma, Myeloma Leuk 2017; 17: 362–369.

Danylesko I Sareli R Bloom-Varda N , et al. Biology of blood and marrow transplantation biosimilar filgrastim (tevagrastim, XMO2) for allogeneic hematopoietic stem cell mobilization and transplantation in patients with acute myelogenous leukemia/myelodysplastic syndromes. Biol Blood Marrow Transplant 2016; 22: 277–283.

Kayikçi O Tekgunduz E Kaya AH , et al. Biosimilar filgrastim (leucostim®) have similar efficacy in steady-state hematopoietic progenitor cell mobilization compared to original filgrastim (neupogen®) and lenograstim (granocyte®): a retrospective multicenter study. Transfus Apher Sci 2017; 56: 832–835.

Sivgin S Karakus E Kaynar L , et al. The comparison of filgrastim (neupogen Ò), biosimilar filgrastim (leucostim Ò) and lenograstim (granocyte Ò) as a first line peripheral blood stem cell mobilization strategy in autologous hematopoieitic stem cell tr. Transfus Apher Sci 2013; 48: 315–320.

Sivgin S Karakus E Keklik M , et al. Evaluation of the efficacy and safety of original filgrastim (neupogen ®), biosimilar filgrastim (leucostim ®) and lenograstim (granocyte ®) in CD34 + peripheral hematopoietic stem cell mobilization procedures for a. Transfus Apher Sci 2016; 54: 410–415.

Tamura K Hashimoto K Nishikawa K. Clinical safety and efficacy of “filgrastim biosimilar 2” in Japanese patients in a post-marketing surveillance study. J Infect Chemother 2018; 24: 363–369.

Gatzemeier U Ciuleanu T Dediu M , et al. XM02, the first biosimilar G-CSF, is safe and effective in reducing the duration of severe neutropenia and incidence of febrile neutropenia in patients with small cell. J Thorac Oncol 2009; 4: 736–740.

Botteri E Krendyukov A Curigliano G. Comparing granulocyte colony e stimulating factor filgrastim and pegfilgrastim to its biosimilars in terms of efficacy and safety : a Meta-analysis of randomised clinical trials in breast cancer patients. Eur J Cancer 2018; 89: 49–55.

Zhou C Huang Y Wang D , et al. A randomized multicenter phase III study of single administration of mecapeg filgrastim (HHPG-19K), a peg fi lgrastim biosimilar, for prophylaxis of Chemotherapy-Induced neutropenia in patients with advanced non e small-cell lung cancer (NSCLC). Clin Lung Cancer 2016; 17: 119–127.

Brokx S Scrocchi L Shah N , et al. Biologicals a demonstration of analytical similarity comparing a proposed biosimilar PEG filgrastim and reference peg filgrastim. Biologicals 2017; 48: 28–38.

Sun D Andayani TM Altyar A , et al. Potential cost savings from chemotherapy-induced febrile neutropenia with biosimilar filgrastim and expanded access to targeted antineoplastic treatment across the European Union G5 countries : a simulation study. Clin Ther 2015; 37: 842–857.

Korkmaz S Altuntas F. Transfusion and apheresis science what is the role of biosimilar G-CSF agents in hematopoietic stem cell mobilization at present? Transfus Apher Sci 2017; 56: 795–799.

Kim WS Buske C Ogura M , et al. Efficacy, pharmacokinetics, and safety of the biosimilar CT-P10 compared with rituximab in patients with previously untreated advanced-stage follicular lymphoma: a randomised, double-blind, parallel-group, non-inferiority phase 3 trial. Lancet Haematol 2017; 4: e362–e373.

Ogura M Sancho JM Cho S , et al. Efficacy, pharmacokinetics, and safety of the biosimilar CT-P10 in comparison with rituximab in patients with previously untreated low-tumour-burden follicular lymphoma: a randomised, double-blind, parallel-group, phase 3 trial. Lancet Haematol 2018; 5: e543–e553.

Jurczak W Moreira I Kanakasetty GB , et al. Rituximab biosimilar and reference rituximab in patients with previously untreated advanced follicular lymphoma (ASSIST-FL): primary results from a confirmatory phase 3, double-blind, randomised, controlled study. Lancet Haematol 2017; 4: e350–e361.

Brain E Caillet P N de G , et al. HER2-targeted treatment for older patients with breast cancer: an expert position paper from the international society of geriatric oncology. J Geriatr Oncol 2019; 10: 1003–1013.

Melo IS Grassi P Ochoa F , et al. N-glycosylation profile analysis of trastuzumab biosimilar candidates by normal phase liquid chromatography and MALDI-TOF MS approaches. J Proteomics 2015; 127: 225–233.

Pivot X Curtit E Lee YJ , et al. A randomized phase I pharmacokinetic study comparing biosimilar candidate SB3 and trastuzumab in healthy male subjects. Clin Ther 2016; 38: 1665–1673. DOI:doi:10.1016/j.clinthera.2016.06.002.

Pivot X Bondarenko I Nowecki Z , et al. A, Phase III study comparing SB3 (a proposed trastuzumab biosimilar) and trastuzumab reference product in HER2-positive early breast cancer treated with neoadjuvant-adjuvant treatment: final safety, immunogenicity and survival results. Eur J Cancer 2018; 93: 19–27.

Pivot X Pegram M Cortes J , et al. Three-year follow-up from a phase 3 study of SB3 (a trastuzumab biosimilar) versus reference trastuzumab in the neoadjuvant setting for human epidermal growth factor receptor 2 e positive breast cancer. Eur J Cancer 2019; 120: 1–9.

Alexeev SM, Khorinko AV, Mukhametshina GZ, et al. Randomized double-blind clinical trial comparing safety and efficacy of the biosimilar BCD-022 with reference trastuzumab. BMC Cancer 2020; 20: 783.

Pivot X Deslypere JP Park LS , et al. A randomized phase I study comparing the pharmacokinetics of HD201, a trastuzumab biosimilar, with european union – sourced herceptin. Clin Ther 2018; 40: 396–405.

Minckwitz G Von Colleoni M Kolberg H , et al. Efficacy and safety of ABP 980 compared with reference trastuzumab in women with HER2-positive early breast cancer (LILAC study): a randomised, double-blind, phase 3 trial. Lancet Oncol 2018; 19: 987–998.

Kolberg H-C Colleoni M Demetriou GS , et al. Cardiac safety of the trastuzumab biosimilar ABP 980 in women with HER2-Positive early breast cancer in the randomized, double-blind, active-controlled LILAC study. Drug Saf 2020; 43: 233–242.

Peraza MA Rule KE Shiue MHI , et al. Nonclinical assessments of the potential biosimilar PF-06439535 and bevacizumab. Regul Toxicol Pharmacol 2018; 95: 236–243.

Romera A Peredpaya S Shparyk Y , et al. Bevacizumab biosimilar BEVZ92 versus reference bevacizumab in combination with FOLFOX or FOLFIRI as first-line treatment for metastatic colorectal cancer : a multicentre, open-label, randomised controlled trial. Lancet Gastroenterol Hepatol 2018; 3: 845–855.

Rezvani H Mortazavizadeh SM Allahyari A , et al. Efficacy and safety of proposed bevacizumab biosimilar BE1040V in patients with metastatic colorectal cancer: a phase III, randomized, double-blind, noninferiority clinical trial. Clin Ther 2020; 42: 848–859.

EMA EMA. Biosimilar, www.ema.europa.eu/en/medicines/field_ema_web_categories%253Aname_field/Human/ema_group_types/ema_medicine/field_ema_med_status/authorised-36/ema_medicine_types/field_ema_med_biosimilar/search_api_aggregation_ema_medicine_types/field_ema_med_biosim (2020, accessed 4 September 2020).

Harston A. How the U. S. Compares to Europe on biosimilar approvals and products in the pipeline, www.biosimilarsip.com/2019/05/07/how-the-u-s-compares-to-europe-on-biosimilar-approvals-and-products-in-the-pipeline-4/ (2019, accessed 24 November 2019).