Clinical impact of drug-drug interactions on abemaciclib in the real-world experience of AB-ITALY study.


Journal

NPJ breast cancer
ISSN: 2374-4677
Titre abrégé: NPJ Breast Cancer
Pays: United States
ID NLM: 101674891

Informations de publication

Date de publication:
17 Jul 2024
Historique:
received: 10 06 2023
accepted: 14 06 2024
medline: 18 7 2024
pubmed: 18 7 2024
entrez: 17 7 2024
Statut: epublish

Résumé

Abemaciclib demonstrated clinical benefit in women affected by HR+/HER2- advanced breast cancer (aBC). Drug-drug interactions (DDIs) can lead to reduced treatment efficacy or increased toxicity. This retro-prospective study aimed to evaluate outcomes, DDIs' impact, and toxicities of abemaciclib combined with endocrine therapy in a real-world setting. Patients from 12 referral Italian hospitals with HR+/HER2- aBC who received abemaciclib were included. Clinical data about comorbidities, concurrent medications, outcomes, and adverse events (AE) were collected. Drug-PIN® (Personalized Interactions Network) is a tool recognizing the role of multiple interactions between active and/or pro-drug forms combined with biochemical and demographic patient data. The software was used to define the Drug-PIN score and Drug-PIN tier (green, yellow, dark yellow, and red) for each patient. Univariate and multivariate analyses were performed to identify predictors of patients' PFS or toxicity. One hundred seventy-three patients were included. 13% of patients had >75years. The overall response rate (ORR) was 63%. The general population's median PFS (mPFS) was 22 months (mo), while mOS were not reached. Patients treated with abemaciclib in combination with AI and fulvestrant had a mPFS of 36 and 19 mo, respectively. The most common toxicities were diarrhea, asthenia, and neutropenia detected in 63%,49%, and 49% of patients. The number of concomitant medications and comorbidities were not associated with survival outcomes (22 vs 17 mo, p = 0.068, p = 0.99). Drug-PIN tier from dark yellow to red and Drug-PIN score >12 were associated with shorter PFS compared to no/low-risk DDIs and score <12 (15 vs 23, p = 0.005, p = 0.0017). Drug interaction was confirmed as an independent biomarker in a multivariate model (p = 0.02). No difference in any grade AE, severe toxicities, and diarrhea were detected among different age subgroups. No association was found between Drug-PIN score or Drug-PIN tier and overall toxicity (p = 0.44), severe AEs (p = 0.11), or drug reduction (p = 0.27). The efficacy and safety of abemaciclib plus ET were confirmed in a real-world setting, even in the elderly population and patients with comorbidities. Evaluation of DDIs with Drug-PIN appears to be an independent predictor of PFS.

Identifiants

pubmed: 39019916
doi: 10.1038/s41523-024-00657-z
pii: 10.1038/s41523-024-00657-z
doi:

Types de publication

Journal Article

Langues

eng

Pagination

58

Informations de copyright

© 2024. The Author(s).

Références

Spring, L. M. et al. Cyclin-dependent kinase 4 and 6 inhibitors for hormone receptor-positive breast cancer: past, present, and future. Lancet 395, 817–827 (2020).
doi: 10.1016/S0140-6736(20)30165-3 pubmed: 32145796
Sledge, G. W. et al. MONARCH 2: abemaciclib in combination with fulvestrant in women with HR+/HER2-advanced breast cancer who had progressed while receiving endocrine therapy. J. Clin. Oncol. 35 (2017).
Sledge, G. W. et al. The effect of abemaciclib plus fulvestrant on overall survival in hormone receptor-positive, ERBB2-negative breast cancer that progressed on endocrine therapy—MONARCH 2: a randomized clinical trial. JAMA Oncol. https://doi.org/10.1001/jamaoncol.2019.4782 (2019).
Kaufman, P. A. et al. Health-related quality of life in MONARCH 2: abemaciclib plus fulvestrant in hormone receptor-positive, HER2-negative advanced breast cancer after endocrine therapy. Oncologist 25, e243–e251 (2020).
doi: 10.1634/theoncologist.2019-0551 pubmed: 32043763
Goetz, M. P. et al. MONARCH 3: abemaciclib as initial therapy for advanced breast cancer. J. Clin. Oncol. https://doi.org/10.1200/JCO.2017.75.6155 (2017).
Goetz, M. P. et al. BREAST CANCER, METASTATIC LBA15 MONARCH 3: interim overall survival (OS) results of abemaciclib plus a nonsteroidal aromatase inhibitor (NSAI) in patients (pts) with HR+, HER2-advanced breast cancer (ABC). https://doi.org/10.1016/j.annonc.2022.08.009 (2022).
Johnston, S. R. D. et al. Abemaciclib combined with endocrine therapy for the adjuvant treatment of HR+, HER2-, node-positive, high-risk, early breast cancer (monarchE). J. Clin. Oncol. 38, 3987–3998 (2020).
doi: 10.1200/JCO.20.02514 pubmed: 32954927 pmcid: 7768339
Goetz, M. P. et al. Safety and efficacy of abemaciclib plus endocrine therapy in older patients with hormone receptor-positive/human epidermal growth factor receptor 2-negative advanced breast cancer: an age-specific subgroup analysis of MONARCH 2 and 3 trials. Breast Cancer Res. Treat. 186, 417–428 (2021).
doi: 10.1007/s10549-020-06029-y pubmed: 33392835 pmcid: 7990838
Howlader, N. et al. US incidence of breast cancer subtypes defined by joint hormone receptor and HER2 status. J. Natl Cancer Inst. 106, https://doi.org/10.1093/jnci/dju055 (2014).
Scotté, F. et al. Addressing the quality of life needs of older patients with cancer: a SIOG consensus paper and practical guide. Ann. Oncol. 29, 1718–1726 (2018).
doi: 10.1093/annonc/mdy228 pubmed: 30010772
Tannenbaum, C. & Sheehan, N. L. Understanding and preventing drug-drug and drug-gene interactions. Expert Rev. Clin. Pharmacol. 7, 533–544 (2014).
doi: 10.1586/17512433.2014.910111 pubmed: 24745854 pmcid: 4894065
Malki, M. A. & Pearson, E. R. Drug-drug-gene interactions and adverse drug reactions. Pharmacogenom. J. 20, 355–366 (2020).
doi: 10.1038/s41397-019-0122-0
Scripture, C. D. & Figg, W. D. Drug interactions in cancer therapy. Nat. Rev. Cancer 6, 546–558 (2006).
doi: 10.1038/nrc1887 pubmed: 16794637
Biganzoli, L. et al. Updated recommendations regarding the management of older patients with breast cancer: a joint paper from the European Society of Breast Cancer Specialists (EUSOMA) and the International Society of Geriatric Oncology (SIOG). Lancet Oncol. 22, e327–e340 (2021).
doi: 10.1016/S1470-2045(20)30741-5 pubmed: 34000244
van Leeuwen, R. W. F. et al. Potential drug interactions in cancer therapy: a prevalence study using an advanced screening method. Ann. Oncol. 22, 2334–2341 (2011).
doi: 10.1093/annonc/mdq761 pubmed: 21343376
Riechelmann, R. P. et al. Potential drug interactions and duplicate prescriptions among cancer patients. J. Natl Cancer Inst. 99, 592–600 (2007).
doi: 10.1093/jnci/djk130 pubmed: 17440160
Groenland, S. L. et al. Clinical pharmacokinetics and pharmacodynamics of the cyclin-dependent kinase 4 and 6 inhibitors palbociclib, ribociclib, and abemaciclib. Clin. Pharmacokinet. 59, 1501–1520 (2020).
doi: 10.1007/s40262-020-00930-x pubmed: 33029704
Slamon, D. J. et al. Overall survival with ribociclib plus fulvestrant in advanced breast cancer. N. Engl. J. Med. 382, 514-524 (2020).
Hortobagyi, G. N. et al. Updated results from MONALEESA-2, a phase III trial of first-line ribociclib plus letrozole versus placebo plus letrozole in hormone receptor-positive, HER2-negative advanced breast cancer. Ann. Oncol. https://doi.org/10.1093/annonc/mdy155 (2018).
Iwata, H. et al. PALOMA-3: phase III trial of fulvestrant with or without palbociclib in premenopausal and postmenopausal women with hormone receptor–positive, human epidermal growth factor receptor 2–negative metastatic breast cancer that progressed on prior endocrine Th. J. Glob. Oncol. https://doi.org/10.1200/jgo.2016.008318 (2017).
Finn, R. S. et al. PALOMA-2: primary results from a phase III trial of palbociclib (P) with letrozole (L) compared with letrozole alone in postmenopausal women with ER+/HER2– advanced breast cancer (ABC). J. Clin. Oncol. https://doi.org/10.1200/jco.2016.34.15_suppl.507 (2016).
Lau, S. W. J. et al. Participation of older adults in clinical trials for new drug applications and biologics license applications from 2010 through 2019. JAMA Netw. Open 5, E2236149 (2022).
doi: 10.1001/jamanetworkopen.2022.36149 pubmed: 36239939 pmcid: 9568796
Fda, Cder & Purdief. Guidance for Industry E7 Studies in Support of Special Populations: Geriatrics Questions and Answers. 800–835 (2012).
Poorvu, P. D. et al. Variation in guideline-concordant care for elderly patients with metastatic breast cancer in the United States. Breast Cancer Res. Treat. 168, 727–737 (2018).
doi: 10.1007/s10549-018-4659-4 pubmed: 29332137
Abdel-Razeq, H., Rous, F. A., Abuhijla, F., Abdel-Razeq, N. & Edaily, S. Breast cancer in geriatric patients: current landscape and future prospects. Clin. Interv. Aging 17, 1445–1460 (2022).
doi: 10.2147/CIA.S365497 pubmed: 36199974 pmcid: 9527811
Vyas, A. M., Aroke, H. & Kogut, S. Guideline-concordant treatment among elderly women with HER2-positive metastatic breast cancer in the United States. JNCCN J. Natl Compr. Cancer Netw. 18, 405–413 (2020).
doi: 10.6004/jnccn.2019.7373
Johnston, S. et al. MONARCH 3 final PFS: a randomized study of abemaciclib as initial therapy for advanced breast cancer. NPJ Breast Cancer 5, https://doi.org/10.1038/s41523-018-0097-z (2019).
Hortobagyi, G. N. et al. Overall survival with ribociclib plus letrozole in advanced breast cancer. N. Engl. J. Med. 386, 942–950 (2022).
doi: 10.1056/NEJMoa2114663 pubmed: 35263519
Posada, M. M. et al. Predicting clinical effects of CYP3A4 modulators on abemaciclib and active metabolites exposure using physiologically based pharmacokinetic modeling. J. Clin. Pharmacol. 60, 915–930 (2020).
doi: 10.1002/jcph.1584 pubmed: 32080863 pmcid: 7318171
Klein, K. & Zanger, U. M. Pharmacogenomics of cytochrome P450 3A4: recent progress toward the ‘missing heritability’ problem. Front. Genetics https://doi.org/10.3389/fgene.2013.00012 (2013).
Budha, N. R. et al. Evaluation of cytochrome P450 3A4-mediated drug-drug interaction potential for cobimetinib using physiologically based pharmacokinetic modeling and simulation. Clin. Pharmacokinet. 55, 1435–1445 (2016).
doi: 10.1007/s40262-016-0412-5 pubmed: 27225997
Roberto, M. et al. Drug-drug interactions and pharmacogenomic evaluation in colorectal cancer patients: the new Drug-PIN® system comprehensive approach. Pharmaceuticals (Basel) 14, 1–12 (2021).
doi: 10.3390/ph14010067
Zhou, S.-F. Drugs behave as substrates, inhibitors and inducers of human cytochrome P450 3A4. Curr. Drug Metab. 9, 310–322 (2008).
doi: 10.2174/138920008784220664 pubmed: 18473749
Sharma, M. et al. Clinical outcomes associated with drug-drug interactions of oral chemotherapeutic agents: a comprehensive evidence-based literature review. Drugs Aging 36, 341–354 (2019).
doi: 10.1007/s40266-019-00640-5 pubmed: 30714077
Spring, L. M., Zangardi, M. L., Moy, B. & Bardia, A. Clinical management of potential toxicities and drug interactions related to cyclin‐dependent kinase 4/6 inhibitors in breast cancer: practical considerations and recommendations. Oncologist https://doi.org/10.1634/theoncologist.2017-0142 (2017).
Drugpin. https://www.drug-pin.com/index.html . Accessed 6 June 2023.
Marcath, L. A., Coe, T. D., Hoylman, E. K., Redman, B. G. & Hertz, D. L. Prevalence of drug-drug interactions in oncology patients enrolled on National Clinical Trials Network oncology clinical trials. BMC Cancer 18, 1155 (2018).
Hertz, D. L., Siden, R., Modlin, J., Gabel, L. L. & Wong, S. F. Drug interaction screening in SWOG clinical trials. Am. J. Health Syst. Pharm. 75, 607 (2018).
doi: 10.2146/ajhp170449 pubmed: 29748299
Johnell, K. & Klarin, I. The relationship between number of drugs and potential drug-drug interactions in the elderly: a study of over 600,000 elderly patients from the Swedish Prescribed Drug Register. Drug Saf. 30, 911–918 (2007).
doi: 10.2165/00002018-200730100-00009 pubmed: 17867728
Franceschi, A. et al. Drug therapeutic failures in emergency department patients: a university hospital experience. Pharmacol. Res. 49, 85–91 (2004).
doi: 10.1016/j.phrs.2003.08.001 pubmed: 14597157
Palleria, C. et al. Pharmacokinetic drug-drug interaction and their implication in clinical management. J. Res. Med. Sci. 18, 601 (2013).
pubmed: 24516494 pmcid: 3897029
Manikandan, P. & Nagini, S. Cytochrome P450 structure, function and clinical significance: a review. Curr. Drug Targets 19, 38-54 (2018).
Beavers, C. J. et al. Cardio-oncology drug interactions: a scientific statement from the American Heart Association. Circulation 145, E811–E838 (2022).
doi: 10.1161/CIR.0000000000001056 pubmed: 35249373
In Vitro Drug Interaction Studies-Cytochrome P450 Enzyme-and Transporter-Mediated Drug Interactions Guidance for Industry. (2020).
Dumbreck, S. et al. Drug-disease and drug-drug interactions: systematic examination of recommendations in 12 UK national clinical guidelines. Br. Med. J. 350, 1–8 (2015).
doi: 10.1136/bmj.h949
Gennari, A. et al. ESMO Clinical Practice Guideline for the diagnosis, staging and treatment of patients with metastatic breast cancer ✰. Ann. Oncol. 32, 1475–1495 (2021).
doi: 10.1016/j.annonc.2021.09.019 pubmed: 34678411
Schwartz, L. H. et al. RECIST 1.1—Update and clarification: from the RECIST committee. Eur. J. Cancer https://doi.org/10.1016/j.ejca.2016.03.081 (2016).
National Institute of Health. National Cancer Institute Common Terminology Criteria for Adverse Events (CTCAE) version 5.0. NIH Publication https://doi.org/10.1080/00140139.2010.489653 (2017).
Occhipinti, M. et al. Evaluation of drug-drug interactions in EGFR-mutated non-small-cell lung cancer patients during treatment with tyrosine-kinase inhibitors. J. Pers. Med. 11, 424 (2021).
Martocchia, A. et al. Comparison of computerized prescription support systems in COVID-19 patients: INTERCheck and Drug-PIN. SN Compr. Clin. Med. 4, 3 (2021).
Salamone, S. et al. Prescription advice based on data of drug-drug-gene interaction of patients with polypharmacy. Pharmgenomics Pers. Med. 15, 765–773 (2022).
pubmed: 36004008 pmcid: 9394521
Borro, M. et al. Individualized drugs’ selection by evaluation of drug properties, pharmacogenomics and clinical parameters: performance of a bioinformatic tool compared to a clinically established counselling process. Pharmgenomics Pers. Med. 14, 955–962 (2021).
pubmed: 34385834 pmcid: 8352633
Preissner, S. H. et al. Machine: comparison of pharmacogenetic expert counselling with a clinical medication support system in a study with 200 genotyped patients. Eur. J. Clin. Pharmacol. 78, 579–587 (2022).
doi: 10.1007/s00228-021-03254-2 pubmed: 34958399
A Distribution-Free Procedure for Comparing Receiver Operating Characteristic Curves from a Paired Experiment on JSTOR. https://www.jstor.org/stable/2337287 . Accessed 29 October 2022.
Zhang, D. D., Zhou, X. H., Freeman, D. H. & Freeman, J. L. A non-parametric method for the comparison of partial areas under ROC curves and its application to large health care data sets. Stat. Med. 21, 701–715 (2002).
doi: 10.1002/sim.1011 pubmed: 11870811

Auteurs

Simone Scagnoli (S)

Department of Radiological, Oncological and Pathological Science, "Sapienza" University of Rome, Rome, Italy.

Simona Pisegna (S)

Department of Experimental Medicine, Sapienza University, Rome, Italy. simona.pisegna@uniroma1.it.

Angela Toss (A)

Department of Oncology and Hematology, Azienda Ospedaliero-Universitaria di Modena, Modena, Italy.
Department of Medical and Surgical Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Roberta Caputo (R)

Department of Breast and Thoracic Oncology, Division of Breast Medical Oncology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Pascale, Naples, Italy.

Michelino De Laurentiis (M)

Department of Breast and Thoracic Oncology, Division of Breast Medical Oncology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Pascale, Naples, Italy.

Michela Palleschi (M)

IRCCS Istituto Romagnolo per lo Studio dei Tumori "Dino Amadori" IRST Meldola IT, Meldola, Italy.

Ugo de Giorgi (U)

IRCCS Istituto Romagnolo per lo Studio dei Tumori "Dino Amadori" IRST Meldola IT, Meldola, Italy.

Enrico Cortesi (E)

Department of Radiological, Oncological and Pathological Science, "Sapienza" University of Rome, Rome, Italy.

Agnese Fabbri (A)

UOC Belcolle Hospital, Viterbo, Italy.

Alessandra Fabi (A)

Precision Medicine in Senology, Department of Women Child and Public Health, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.
Precision Medicine in Senology, Scientific Directorate, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.

Ida Paris (I)

Division of Gynecologic Oncology, Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, Rome, Italy.

Armando Orlandi (A)

Fondazione Policlinico Universitario Agostino Gemelli IRCCS Comprehensive Cancer Center, Unit of Medical Oncology, Rome, Italy.

Giuseppe Curigliano (G)

Division of New Drugs and Early Drug Development for Innovative Therapies, European Institute of Oncology, IRCCS, Milan, Italy.

Carmen Criscitiello (C)

Department of Oncology and Hematology (DIPO), University of Milan, Milan, Italy.

Ornella Garrone (O)

Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, SC Oncologia Medica, Milan, Italy.

Gianluca Tomasello (G)

Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, SC Oncologia Medica, Milan, Italy.

Giuliana D'Auria (G)

Sandro Pertini Hospital Unit of Medical Oncology, Rome, Italy.

Patrizia Vici (P)

Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Istituto Nazionale Tumori Regina Elena, UOSD Sperimentazioni di fase IV IT, Rome, Italy.

Enrico Ricevuto (E)

University of L'Aquila, L'Aquila, Italy.

Federica Domati (F)

Department of Medical and Surgical Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Claudia Piombino (C)

Department of Oncology and Hematology, Azienda Ospedaliero-Universitaria di Modena, Modena, Italy.

Sara Parola (S)

Department of Breast and Thoracic Oncology, Division of Breast Medical Oncology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Pascale, Naples, Italy.

Roberta Scafetta (R)

Università Campus Biomedico, Rome, Italy.

Alessio Cirillo (A)

Department of Radiological, Oncological and Pathological Science, "Sapienza" University of Rome, Rome, Italy.
Department of Experimental Medicine, Sapienza University, Rome, Italy.

Beatrice Taurelli Salimbeni (B)

Division of New Drugs and Early Drug Development for Innovative Therapies, European Institute of Oncology, IRCCS, Milan, Italy.

Francesca Sofia Di Lisa (FS)

Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Istituto Nazionale Tumori Regina Elena, UOSD Sperimentazioni di fase IV IT, Rome, Italy.

Lidia Strigari (L)

IRCSS AOU Bologna, Bologna, Italy.

Robert Preissner (R)

Institute of Physiology and Science-IT, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Maurizio Simmaco (M)

Laboratory of Clinical Biochemistry, Sant'Andrea University Hospital, Rome, Italy.
Department of Neurosciences, Mental Health and Sensory Organs (NESMOS), Sapienza University of Rome, Rome, Italy.

Daniele Santini (D)

Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome, Rome, Italy.
Medical Oncology A, AOU Policlinico Umberto I, Rome, Italy.

Paolo Marchetti (P)

Istituto Dermopatico dell'Immacolata IRCCS, Rome, Italy.

Andrea Botticelli (A)

Department of Radiological, Oncological and Pathological Science, "Sapienza" University of Rome, Rome, Italy.

Classifications MeSH