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BLOOD RESEARCH September 2020 ARTICLE VOLUME 55ㆍNUMBER 3 ORIGINAL BLOOD RESEARCH September 2020 ARTICLE Use of generic imatinib as first-line treatment in patients with chronic myeloid leukemia (CML): the GIMS (Glivec to Imatinib Switch) study Maria Gemelli1#, Elena Maria Elli2#, Chiara Elena3, Alessandra Iurlo4, Tamara Intermesoli5, Margherita Maffioli6, Ester Pungolino7, Maria Cristina Carraro8, Mariella D’Adda9, Francesca Lunghi10, Michela Anghileri11, Nicola Polverelli12, Marianna Rossi13, Mattia Bacciocchi14, Elisa Bono3, Cristina Bucelli4, Francesco Passamonti6, Laura Antolini15, Carlo Gambacorti-Passerini2,14 1Oncology Unit, San Gerardo Hospital, ASST-Monza, 2Hematology Division and Bone Marrow Unit, Ospedale San Gerardo, ASST- Monza, Monza, 3Division of Hematology, Fondazione IRCCS Policlinico San Matteo, Pavia, 4Hematology Division, Foundation IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, 5Hematology and Bone Marrow Transplant Unit, ASST Papa Giovanni XXIII, Bergamo, 6Hematology Unit, Ospedale di Circolo, Varese, 7Division of Hematology, ASST Grande Ospedale Metropolitano Niguarda, Milano, 8Hematology and Transfusional Medicine Unit, ASST Fatebenefratelli Sacco, Milan, 9Department of Hematology, ASST Spedali Civili di Brescia, Brescia, 10Hematology and Bone Marrow Transplantation Unit, San Raffaele Scientific Institute, IRCCS Milano, 11Oncology Department, ASST Lecco, Lecco, 12Chair of Hematology, Unit of Blood Diseases and Stem Cell Transplantation, University of Brescia, ASST Spedali Civili di Brescia, Brescia, 13Department of Hematology, Cancer Center, IRCCS Humanitas Research Hospital/Humanitas University, Rozzano, 14Department of Medicine and Surgery, University of Milano-Bicocca, 15Center of Biostatistics for Clinical Epidemiology, Department of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy p-ISSN 2287-979X / e-ISSN 2288-0011 Background https://doi.org/10.5045/br.2020.2020130 Generic formulations of imatinib mesylate have been introduced in Western Europe since Blood Res 2020;55:139-145. 2017 to treat patients with chronic myeloid leukemia (CML). However, results on the safety and efficacy of generic formulations are contrasting. The aim of this study was to Received on June 5, 2020 investigate the safety and efficacy of generic imatinib in CML patients treated in 12 Italian Revised on July 14, 2020 institutes. Accepted on July 24, 2020 Methods This is an observational, retro-prospective analysis of patients with CML for whom the #These authors contributed equally to this treatment was switched from brand to generic imatinib. We analyzed and compared the work. variation in quantitative PCR values before and after the switch, and the proportion of patients who maintained molecular response after changing from brand to generic imatinib. Adverse events (AEs) were also evaluated. Results Two hundred patients were enrolled. The median PCR value after the switch was reduced by 0.25 compared to the values before the switch. A significant difference was found be- tween median PCR values before and after the switch in favor of generic imatinib (P= 0.003). Molecular responses remained stable in 69.0%, improved in 25.5%, and wors- ened in 5.5% of patients. AEs were similar in the pre- and post-switch periods; however, a significant difference was found in favor of generic imatinib for muscular cramps (P＜ 0.0001), periorbital edema (P=0.0028), edema of the limbs (P＜0.0001), fatigue (P=0.0482), and diarrhea (P=0.0027). Correspondence to Carlo Gambacorti-Passerini, Ph.D. Conclusion Department of Medicine and Surgery, Our data indicate that generic imatinib does not have deleterious effects on CML control University of Milano-Bicocca, Via Cadore and present an acceptable safety profile, similar or better than brand imatinib. 48, 20900, Monza (MB), Italy E-mail: [email protected] Key Words Imatinib, Generic, Chronic myeloid leukemia, Generic imatinib, BCR/ABL, Ⓒ 2020 Korean Society of Hematology Adverse events This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 140 Maria Gemelli, et al. Western Europe. INTRODUCTION However, owing to these contrasting results, assessing the safety and efficacy of available generic formulations is of Chronic myeloid leukemia (CML) is a rare disease charac- paramount importance. Furthermore, some patient associa- terized by the presence of the Philadelphia chromosome tions and clinicians are doubtful about a switch to the generic (Ph+) [1]. In 2001, the Food and Drug Administration (FDA) one for fear of disease worsening and higher side effects approved imatinib mesylate (Glivec, Novartis, Klybeckstrasse, [17-19]. For these reasons, it is necessary to further assess Basel, Switzerland), a first-generation BCR-ABL tyrosine- the efficacy and safety of new generic formulations in larger kinase inhibitor (TKI), for the treatment of CML on the and prospective trials. basis of the results of two phase 2 studies showing better hematologic and cytogenetic responses in both chronic (CP) MATERIALS AND METHODS and accelerated (AP) phases. Based on the result of the phase 3 IRIS trial, imatinib became the new standard of care for first-line therapy [2, 3]. Imatinib dramatically changed the This is an observational, multicenter, retro-prospective prognosis of CML patients, ensuring a life expectancy com- analysis of patients with CML in the CP with stable disease parable to that of the general population, with deaths more [defined as at least 18 months of complete cytogenetic re- likely due to comorbidities than due to CML [4]. Despite sponse (CCyR) and 36 months of treatment with branded this, most patients require continuing imatinib treatment imatinib] who had their treatment switched from branded lifelong because of the persistence of quiescent leukemic to generic imatinib since January 2017 in 12 Italian Institutes clones [5]. The expiration date of market patents vary among belonging to the REL (Lombardy Hematological Network). countries, and bioequivalence data are sufficient to obtain Previous treatments with interferon or oncocarbide were approval for generic drugs from regulatory entities. In partic- allowed if administered for a maximum of one month for ular, a difference in bioavailability in the range of 80–125% cytoreductive purpose. Patients in the AP or BP at the time for branded imatinib (Glivec) is considered acceptable [6]. of enrollment were excluded, as well as patients the in second Since 2012, generic formulations of imatinib were approved or subsequent lines of treatment. Five manufacturers of ge- in Europe, Canada, and United States on the basis of data neric imatinib were used during this period: Accord, Sandoz, showing bioequivalence between generic and branded im- Teva, Dr. Reddy, Mylan; accord accounted for more than atinib [7-9]. In Italy, the first generic imatinib was approved 50% of total usage. We analyzed the variation in quantitative by Agenzia Italiana del Farmaco (AIFA) in January 2017. PCR values, considering BCR/ABL cDNA copies/≥10,000 However, some formulations were available in other coun- ABL copies corrected by the International Standard (IS). tries before official patent expiration. Despite this, there Three PCR values were considered in a period of 12 months is a lack of solid data on the efficacy of generic imatinib. before the switch and 3 values in the 12 months after the In the literature, only small, retrospective studies, conducted switch (this period was then modified in 20 months consider- in countries with easier approval rules, are available. Some ing that, in clinical practice, patients with stable disease case reports documented loss of molecular and cytogenetic were often evaluated for PCR with a six-month interval). responses with risk of progression from CP to AP after the PCR tests were performed at each center. Molecular re- switch to generic imatinib, which was reverted with the sponses were assessed for each PCR value and defined as reintroduction of the branded formulation in most cases follows: molecular response (MR) 3 if transcript levels were [10-12]. Saavedra et al. [13] reported four out of eight patients ≤0.1% BCR-ABL/ABL, MR4 if ≤0.01% BCR-ABL/ABL, who switched to generic imatinib and lost cytogenetic re- MR4.5 if ≤0.0032%, and MR5 if ≤0.001%. We evaluated sponse within three to four months since the switch, and and compared the median PCR values before and after the all the eight patients had to switch to second-generation switch as well as the proportion of patients who maintained, TKI due to disease progression or AEs. In another prospective improved, or worsened their molecular response, and the single-center Iraqi study among 126 CML patients in the AEs encountered by the patients with branded and generic CP who were first treated with branded imatinib and then formulations; AEs were recorded according to the 3 main switched to generic imatinib, many patients lost their hema- AEs declared by the patient and registered by the treating tologic response and had problems with tolerability; all pa- physician. AEs were graded according to the Common tients were switched back to the branded imatinib [14]. Terminology Criteria for AEs (CTCAE) 4.0. Wilcoxon Conversely, in a retrospective analysis from Latvia, sec- non-parametric test for individual paired data was used to ond-generation
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