Towards clinical adherence monitoring of oral endocrine breast cancer therapies by LC-HRMS-method development, validation, comparison of four sample matrices, and proof of concept.

Adherence monitoring Bioanalysis Breast cancer LC-HRMS Sample matrices

Journal

Analytical and bioanalytical chemistry
ISSN: 1618-2650
Titre abrégé: Anal Bioanal Chem
Pays: Germany
ID NLM: 101134327

Informations de publication

Date de publication:
15 Mar 2024
Historique:
received: 18 12 2023
accepted: 06 03 2024
revised: 05 03 2024
medline: 15 3 2024
pubmed: 15 3 2024
entrez: 15 3 2024
Statut: aheadofprint

Résumé

Oral endocrine therapies (OET) for breast cancer treatment need to be taken over a long period of time and are associated with considerable side effects. Therefore, adherence to OET is an important issue and of high clinical significance for breast cancer patients' caregivers. We hypothesized that a new bioanalytical strategy based on liquid chromatography and high-resolution mass spectrometry might be suitable for unbiased adherence monitoring (AM) of OET. Four different biomatrices (plasma, urine, finger prick blood by volumetric absorptive microsampling (VAMS), oral fluid (OF)) were evaluated regarding their suitability for AM of the OET abemaciclib, anastrozole, exemestane, letrozole, palbociclib, ribociclib, tamoxifen, and endoxifen. An analytical method was developed and validated according to international recommendations. The analytical procedures were successfully validated in all sample matrices for most analytes, even meeting requirements for therapeutic drug monitoring. Chromatographic separation of analytes was achieved in less than 10 min and limits of quantification ranged from 1 to 1000 ng/mL. The analysis of 25 matching patient samples showed that AM of OET is possible using all four matrices with the exception of, e.g., letrozole and exemestane in OF. We were able to show that unbiased bioanalytical AM of OET was possible using different biomatrices with distinct restrictions. Sample collection of VAMS was difficult in most cases due to circulatory restraints and peripheral neuropathy in fingers and OF sampling was hampered by dry mouth syndrome in some cases. Although parent compounds could be detected in most of the urine samples, metabolites should be included when analyzing urine or OF. Plasma is currently the most suitable matrix due to available reference concentrations.

Identifiants

pubmed: 38488952
doi: 10.1007/s00216-024-05244-6
pii: 10.1007/s00216-024-05244-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

WHO. Breast cancer 2023 https://www.who.int/news-room/fact-sheets/detail/breast-cancer .
Paranjpe R, John G, Trivedi M, Abughosh S. Identifying adherence barriers to oral endocrine therapy among breast cancer survivors. Breast Cancer Res Treat. 2019;174(2):297–305. https://doi.org/10.1007/s10549-018-05073-z .
doi: 10.1007/s10549-018-05073-z pubmed: 30523459
Chlebowski RT, Geller ML. Adherence to endocrine therapy for breast cancer. Oncology. 2006;71(1–2):1–9. https://doi.org/10.1159/000100444 .
doi: 10.1159/000100444 pubmed: 17344666
Kardas P, Lewek P, Matyjaszczyk M. Determinants of patient adherence: a review of systematic reviews. Front Pharmacol. 2013;4:91. https://doi.org/10.3389/fphar.2013.00091 .
doi: 10.3389/fphar.2013.00091 pubmed: 23898295 pmcid: 3722478
Partridge AH, Wang PS, Winer EP, Avorn J. Nonadherence to adjuvant tamoxifen therapy in women with primary breast cancer. J Clin Oncol. 2003;21(4):602–6. https://doi.org/10.1200/JCO.2003.07.071 .
doi: 10.1200/JCO.2003.07.071 pubmed: 12586795
WHO. Adherence to long-term therapies: evidence for action. 2003 https://www.who.int/chp/knowledge/publications/adherence_report/en/
Jacobs CM, Wagmann L, Meyer MR. Sample matrices for mass spectrometry-based adherence monitoring: a systematic critical review. Ther Drug Monit. 2023;epub ahead of print. https://doi.org/10.1097/FTD.0000000000001145
Rentsch KM. Knowing the unknown – state of the art of LCMS in toxicology. TrAC Trends Anal Chem. 2016;84:88–93. https://doi.org/10.1016/j.trac.2016.01.028 .
doi: 10.1016/j.trac.2016.01.028
Gupta P, Patel P, Strauch B, Lai FY, Akbarov A, Gulsin GS, et al. Biochemical screening for nonadherence is associated with blood pressure reduction and improvement in adherence. Hypertension. 2017;70(5):1042–8. https://doi.org/10.1161/HYPERTENSIONAHA.117.09631 .
doi: 10.1161/HYPERTENSIONAHA.117.09631 pubmed: 28847892
Richter LHJ, Jacobs CM, Mahfoud F, Kindermann I, Bohm M, Meyer MR. Development and application of a LC-HRMS/MS method for analyzing antihypertensive drugs in oral fluid for monitoring drug adherence. Anal Chim Acta. 2019;1070:69–79. https://doi.org/10.1016/j.aca.2019.04.026 .
doi: 10.1016/j.aca.2019.04.026 pubmed: 31103169
Jacobs CM, Kunz M, Mahfoud F, Wagmann L, Meyer MR. Evaluation and analytical applicability of a novel volumetric absorptive microsampling strategy for adherence monitoring of antihypertensive drugs by means of LC-HRMS/MS. Anal Chim Acta. 2021;1187:339137. https://doi.org/10.1016/j.aca.2021.339137 .
doi: 10.1016/j.aca.2021.339137 pubmed: 34753562
Jacobs CM, Wagmann L, Meyer MR. Development, validation, and application of a quantitative volumetric absorptive microsampling-based method in finger prick blood by means of LC-HRMS/MS applicable for adherence monitoring of antipsychotics. Anal Bioanal Chem. 2021;413(6):1729–37. https://doi.org/10.1007/s00216-020-03143-0 .
doi: 10.1007/s00216-020-03143-0 pubmed: 33517479 pmcid: 7921024
Schulz M, Schmoldt A, Andresen-Streichert H, Iwersen-Bergmann S. Revisited: therapeutic and toxic blood concentrations of more than 1100 drugs and other xenobiotics. Crit Care. 2020;24(1):195. https://doi.org/10.1186/s13054-020-02915-5 .
doi: 10.1186/s13054-020-02915-5 pubmed: 32375836 pmcid: 7201985
Jung O, Gechter JL, Wunder C, Paulke A, Bartel C, Geiger H, et al. Resistant hypertension? Assessment of adherence by toxicological urine analysis. J Hypertens. 2013;31(4):766–74. https://doi.org/10.1097/HJH.0b013e32835e2286 .
doi: 10.1097/HJH.0b013e32835e2286 pubmed: 23337469
Lawson AJ, Shipman KE, George S, Dasgupta I. A novel ‘dilute-and-shoot’ liquid chromatography-tandem mass spectrometry method for the screening of antihypertensive drugs in urine. J Anal Toxicol. 2016;40(1):17–27. https://doi.org/10.1093/jat/bkv102 .
doi: 10.1093/jat/bkv102 pubmed: 26333988
De Nicolo A, Avataneo V, Rabbia F, Sciandra M, Tosello F, Cusato J, et al. UHPLC-MS/MS method with sample dilution to test therapeutic adherence through quantification of ten antihypertensive drugs in urine samples. J Pharm Biomed Anal. 2017;142:279–85. https://doi.org/10.1016/j.jpba.2017.05.018 .
doi: 10.1016/j.jpba.2017.05.018 pubmed: 28538203
Ritscher S, Hoyer M, Wunder C, Obermuller N, Toennes SW. Evaluation of the dose-related concentration approach in therapeutic drug monitoring of diuretics and beta-blockers - drug classes with low adherence in antihypertensive therapy. Sci Rep. 2019;9(1):15652. https://doi.org/10.1038/s41598-019-52164-y .
doi: 10.1038/s41598-019-52164-y pubmed: 31666620 pmcid: 6821771
Braal CL, Jongbloed EM, Wilting SM, Mathijssen RHJ, Koolen SLW, Jager A. Inhibiting CDK4/6 in breast cancer with palbociclib, ribociclib, and abemaciclib: similarities and differences. Drugs. 2021;81(3):317–31. https://doi.org/10.1007/s40265-020-01461-2 .
doi: 10.1007/s40265-020-01461-2 pubmed: 33369721
Guideline on bioanalytical method validation, EMEA/CHMP/EWP/192217/2009. Rev.1 Corr.2 2011. https://www.ema.europa.eu/en/documents/scientific-guideline/guideline-bioanalytical-method-validation_en.pdf .
ICH guideline M10 on bioanalytical method validation and study sample analysis, EMA/CHMP/ICH/172948/2019. 2022. https://www.ema.europa.eu/en/documents/scientific-guideline/ich-guideline-m10-bioanalytical-method-validation-step-5_en.pdf
Posocco B, Buzzo M, Poetto AS, Orleni M, Gagno S, Zanchetta M, et al. Simultaneous quantification of palbociclib, ribociclib and letrozole in human plasma by a new LC-MS/MS method for clinical application. PLoS One. 2020;15(2):e0228822. https://doi.org/10.1371/journal.pone.0228822 .
doi: 10.1371/journal.pone.0228822 pubmed: 32032379 pmcid: 7006908
Poetto AS, Posocco B, Gagno S, Orleni M, Zanchetta M, Iacuzzi V, et al. A new dried blood spot LC-MS/MS method for therapeutic drug monitoring of palbociclib, ribociclib, and letrozole in patients with cancer. J Chromatogr B Analyt Technol Biomed Life Sci. 2021;1185:122985. https://doi.org/10.1016/j.jchromb.2021.122985 .
doi: 10.1016/j.jchromb.2021.122985 pubmed: 34700133
Martinez-Chavez A, Rosing H, Hillebrand M, Tibben M, Schinkel AH, Beijnen JH. Development and validation of a bioanalytical method for the quantification of the CDK4/6 inhibitors abemaciclib, palbociclib, and ribociclib in human and mouse matrices using liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem. 2019;411(20):5331–45. https://doi.org/10.1007/s00216-019-01932-w .
doi: 10.1007/s00216-019-01932-w pubmed: 31209549 pmcid: 6647725
Habler K, Kalla AS, Rychlik M, Vogeser M, Teupser D. Therapeutic drug monitoring in breast cancer therapy - LC-MS/MS method for quantification of the CDK4/6 inhibitors abemaciclib, palbociclib, ribociclib, and major metabolites abemaciclib M20 and M2 in human serum. J Pharm Biomed Anal. 2023;225:115211. https://doi.org/10.1016/j.jpba.2022.115211 .
doi: 10.1016/j.jpba.2022.115211 pubmed: 36603395
Capiau S, Veenhof H, Koster RA, Bergqvist Y, Boettcher M, Halmingh O, et al. Official International Association for Therapeutic Drug Monitoring and Clinical Toxicology guideline: development and validation of dried blood spot-based methods for therapeutic drug monitoring. Ther Drug Monit. 2019;41(4):409–30. https://doi.org/10.1097/FTD.0000000000000643 .
doi: 10.1097/FTD.0000000000000643 pubmed: 31268966
Denniff P, Spooner N. Volumetric absorptive microsampling: a dried sample collection technique for quantitative bioanalysis. Anal Chem. 2014;86(16):8489–95. https://doi.org/10.1021/ac5022562 .
doi: 10.1021/ac5022562 pubmed: 25058158
Koster RA, Niemeijer P, Veenhof H, Hateren KV, Alffenaar JC, Touw DJ. A volumetric absorptive microsampling LC-MS/MS method for five immunosuppressants and their hematocrit effects. Bioanalysis. 2019;11(6):495–508. https://doi.org/10.4155/bio-2018-0312 .
doi: 10.4155/bio-2018-0312 pubmed: 30892068
Baselt RC. Disposition of toxic drugs and chemicals in man. 11th ed. Seal Beach, CA: Biomedical Publications; 2017. p. 2017.
Groenland SL, van Nuland M, Verheijen RB, Schellens JHM, Beijnen JH, Huitema ADR, et al. Therapeutic drug monitoring of oral anti-hormonal drugs in oncology. Clin Pharmacokinet. 2019;58(3):299–308. https://doi.org/10.1007/s40262-018-0683-0 .
doi: 10.1007/s40262-018-0683-0 pubmed: 29862467
Sanchez-Spitman AB, Swen JJ, Dezentje VO, Moes D, Gelderblom H, Guchelaar HJ. Clinical pharmacokinetics and pharmacogenetics of tamoxifen and endoxifen. Expert Rev Clin Pharmacol. 2019;12(6):523–36. https://doi.org/10.1080/17512433.2019.1610390 .
doi: 10.1080/17512433.2019.1610390 pubmed: 31008668
Nilsson LB, Eklund G. Direct quantification in bioanalytical LC-MS/MS using internal calibration via analyte/stable isotope ratio. J Pharm Biomed Anal. 2007;43(3):1094–9. https://doi.org/10.1016/j.jpba.2006.09.030 .
doi: 10.1016/j.jpba.2006.09.030 pubmed: 17084056
Stokvis E, Rosing H, Beijnen JH. Stable isotopically labeled internal standards in quantitative bioanalysis using liquid chromatography/mass spectrometry: necessity or not? Rapid Commun Mass Spectrom. 2005;19(3):401–7. https://doi.org/10.1002/rcm.1790 .
doi: 10.1002/rcm.1790 pubmed: 15645520
Capiau S, Stove C. Hematocrit prediction in volumetric absorptive microsamples. J Pharm Biomed Anal. 2020;190:113491. https://doi.org/10.1016/j.jpba.2020.113491 .
doi: 10.1016/j.jpba.2020.113491 pubmed: 32777731
Jayaraman S, Reid JM, Hawse JR, Goetz MP. Endoxifen, an estrogen receptor targeted therapy: from bench to bedside. Endocrinology. 2021;162(12). https://doi.org/10.1210/endocr/bqab191.
Beverage JN, Sissung TM, Sion AM, Danesi R, Figg WD. CYP2D6 polymorphisms and the impact on tamoxifen therapy. J Pharm Sci. 2007;96(9):2224–31. https://doi.org/10.1002/jps.20892 .
doi: 10.1002/jps.20892 pubmed: 17518364
Peeters LEJ, Feyz L, Boersma E, Daemen J, van Gelder T, Koch BCP, et al. Clinical applicability of monitoring antihypertensive drug levels in blood. Hypertension. 2020;76(1):80–6. https://doi.org/10.1161/HYPERTENSIONAHA.120.15038 .
doi: 10.1161/HYPERTENSIONAHA.120.15038 pubmed: 32418497
Dash RP, Veeravalli V, Thomas JA, Rosenfeld C, Mehta N, Srinivas NR. Whole blood or plasma: what is the ideal matrix for pharmacokinetic-driven drug candidate selection? Future Med Chem. 2021;13(2):157–71. https://doi.org/10.4155/fmc-2020-0187 .
doi: 10.4155/fmc-2020-0187 pubmed: 33275044
Biagiotti S, Pirla E, Magnani M. Drug transport by red blood cells. Front Physiol. 2023;14:1308632. https://doi.org/10.3389/fphys.2023.1308632 .
doi: 10.3389/fphys.2023.1308632 pubmed: 38148901 pmcid: 10750411
Chen G, Jirjees F Sr, Al Bawab A, McElnay JC. Quantification of amlodipine in dried blood spot samples by high performance liquid chromatography tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2018;1072:252–8. https://doi.org/10.1016/j.jchromb.2017.11.018 .
doi: 10.1016/j.jchromb.2017.11.018 pubmed: 29195144
Jacobs CM, Kunz M, Mahfoud F, Wagmann L, Meyer MR. Closing the gap - development of an analytical methodology using volumetric absorptive microsampling of finger prick blood followed by LC-HRMS/MS for adherence monitoring of antihypertensive drugs. Anal Bioanal Chem. 2023;415(1):167–77. https://doi.org/10.1007/s00216-022-04394-9 .
doi: 10.1007/s00216-022-04394-9 pubmed: 36318313

Auteurs

Cathy M Jacobs (CM)

Department of Experimental and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Center for Molecular Signaling (PZMS), Saarland University, Homburg, Germany.

Julia C Radosa (JC)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Lea Wagmann (L)

Department of Experimental and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Center for Molecular Signaling (PZMS), Saarland University, Homburg, Germany.

Julia S M Zimmermann (JSM)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Askin C Kaya (AC)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Aylin Aygün (A)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Tatjana Edel (T)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Lisa Stotz (L)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Mohamed Ismaeil (M)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Erich-Franz Solomayer (EF)

Department of Gynecology, Obstetrics and Reproductive Medicine, Saarland University Hospital, Homburg, Saarland, Germany.

Markus R Meyer (MR)

Department of Experimental and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Center for Molecular Signaling (PZMS), Saarland University, Homburg, Germany. markus.meyer@uks.eu.

Classifications MeSH