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Review

Next-generation sequencing in pharmacogenomics – fit for clinical decision support?

ORCID Icon & ORCID Icon
Pages 213-223 | Received 16 Oct 2023, Accepted 16 Jan 2024, Published online: 23 Jan 2024

References

  • Sim SC, Kacevska M, Ingelman-Sundberg M. Pharmacogenomics of drug-metabolizing enzymes: a recent update on clinical implications and endogenous effects. Pharmacogenomics J. 2013;13(1):1–11. doi: 10.1038/tpj.2012.45
  • Weinshilboum RM, Wang L. Pharmacogenomics: precision medicine and drug response. Mayo Clin Proc. 2017;92(11):1711–1722. doi: 10.1016/j.mayocp.2017.09.001
  • Lauschke VM, Zhou Y, Ingelman-Sundberg M. Novel genetic and epigenetic factors of importance for inter-individual differences in drug disposition, response and toxicity. Pharmacol Ther. 2019;197:122–152. doi: 10.1016/j.pharmthera.2019.01.002
  • Pirmohamed M. Pharmacogenomics: current status and future perspectives. Nat Rev Genet. 2023;24(6):350–362. doi: 10.1038/s41576-022-00572-8
  • Shekhani R, Steinacher L, Swen JJ, et al. Evaluation of current regulation and guidelines of pharmacogenomic drug labels: opportunities for improvements. Clin Pharmacol Ther. 2020;107(5):1240–1255. doi: 10.1002/cpt.1720
  • Driest SLV, Shi Y, Bowton EA, et al. Clinically actionable genotypes among 10,000 patients with preemptive pharmacogenomic testing. Clin Pharmacol Ther. 2014;95(4):423–431. doi: 10.1038/clpt.2013.229
  • Reisberg S, Krebs K, Lepamets M, et al. Translating genotype data of 44,000 biobank participants into clinical pharmacogenetic recommendations: challenges and solutions. Genet Med. 2019;21(6):1345–1354. doi: 10.1038/s41436-018-0337-5
  • McInnes G, Lavertu A, Sangkuhl K, et al. Pharmacogenetics at scale: an analysis of the UK biobank. Clin Pharmacol Ther. 2021;109(6):1528–1537. doi: 10.1002/cpt.2122
  • Kimpton JE, Carey IM, Threapleton CJD, et al. Longitudinal exposure of English primary care patients to pharmacogenomic drugs: an analysis to inform design of pre‐emptive pharmacogenomic testing. Br J Clin Pharmacol. 2019;85(12):2734–2746. doi: 10.1111/bcp.14100
  • Hayward J, McDermott J, Qureshi N, et al. Pharmacogenomic testing to support prescribing in primary care: a structured review of implementation models. Pharmacogenomics. 2021;22(12):761–776. doi: 10.2217/pgs-2021-0032
  • Lauschke VM, Ingelman-Sundberg M. Prediction of drug response and adverse drug reactions: from twin studies to next generation sequencing. Eur J Pharm Sci. 2019;130:65–77. doi: 10.1016/j.ejps.2019.01.024
  • Jukic MM, Smith RL, Haslemo T, et al. Effect of CYP2D6 genotype on exposure and efficacy of risperidone and aripiprazole: a retrospective, cohort study. Lancet Psychiatry. 2019;6(5):418–426. doi: 10.1016/S2215-0366(19)30088-4
  • Bråten LS, Haslemo T, Jukic MM, et al. Impact of CYP2C19 genotype on sertraline exposure in 1200 scandinavian patients. Neuropsychopharmacol. 2020;45(3):570–576. doi: 10.1038/s41386-019-0554-x
  • Lauschke VM, Zhou Y, Ingelman-Sundberg M. Pharmacogenomics beyond single common genetic variants: the way forward. Annu Rev Pharmacol Toxicol. 2023;64. doi: 10.1146/annurev-pharmtox-051921-091209. Online ahead of print.
  • Ingelman-Sundberg M, Mkrtchian S, Zhou Y, et al. Integrating rare genetic variants into pharmacogenetic drug response predictions. Hum Genomics. 2018;12(1):26. doi: 10.1186/s40246-018-0157-3
  • Wright GEB, Carleton B, Hayden MR, et al. The global spectrum of protein-coding pharmacogenomic diversity. Pharmacogenomics J. 2018;18(1):187–195. doi: 10.1038/tpj.2016.77
  • Schärfe CPI, Tremmel R, Schwab M, et al. Genetic variation in human drug-related genes. Genome Med. 2017;9(1):117. doi: 10.1186/s13073-017-0502-5
  • Kozyra M, Ingelman-Sundberg M, Lauschke VM. Rare genetic variants in cellular transporters, metabolic enzymes, and nuclear receptors can be important determinants of interindividual differences in drug response. Genet Med. 2017;19(1):20–29. doi: 10.1038/gim.2016.33
  • Tremmel R, Zhou Y, Schwab M, et al. Structural variation of the coding and non-coding human pharmacogenome. NPJ Genom Med. 2023;8(1):24. doi: 10.1038/s41525-023-00371-y
  • Dunnenberger HM, Crews KR, Hoffman JM, et al. Preemptive clinical pharmacogenetics implementation: Current programs in five US medical centers. Annu Rev Pharmacol Toxicol. 2015;55(1):89–106. doi: 10.1146/annurev-pharmtox-010814-124835
  • Krebs K, Milani L. Translating pharmacogenomics into clinical decisions: do not let the perfect be the enemy of the good. Hum Genomics. 2019;13(1):39. doi: 10.1186/s40246-019-0229-z
  • Duarte JD, Dalton R, Elchynski AL, et al. Multisite investigation of strategies for the clinical implementation of pre-emptive pharmacogenetic testing. Genet Med. 2021;23(12):2335–2341. doi: 10.1038/s41436-021-01269-9
  • Yang W, Wu G, Broeckel U, et al. Comparison of genome sequencing and clinical genotyping for pharmacogenes. Clin Pharmacol Ther. 2016;100(4):380–388. doi: 10.1002/cpt.411
  • Chua EW, Cree SL, Ton KNT, et al. Cross-Comparison of exome analysis, next-generation sequencing of amplicons, and the iPLEX ADME PGx panel for pharmacogenomic profiling. Front Pharmacol. 2016;7:1. doi: 10.3389/fphar.2016.00001
  • Rasmussen-Torvik LJ, Almoguera B, Doheny KF, et al. Concordance between research sequencing and clinical pharmacogenetic genotyping in the eMERGE-PGx study. J Mol Diagn. 2017;19(4):561–566. doi: 10.1016/j.jmoldx.2017.04.002
  • Lopes JL, Harris K, Karow MB, et al. Targeted genotyping in clinical pharmacogenomics what is missing? J Mol Diagn. 2022;24(3):253–261. doi: 10.1016/j.jmoldx.2021.11.008
  • Lauschke VM, Milani L, Ingelman-Sundberg M. Pharmacogenomic biomarkers for improved drug therapy—recent progress and future developments. AAPS J. 2017;20(1):4. doi: 10.1208/s12248-017-0161-x
  • Desta Z, El‐Boraie A, Gong L, et al. PharmVar GeneFocus: CYP2B6. Clin Pharmacol Ther. 2021;110(1):82–97. doi: 10.1002/cpt.2166
  • Schaal W, Ameur A, Olsson-Strömberg U, et al. Migrating to long-read sequencing for clinical routine BCR-ABL1 TKI resistance mutation screening. Cancer Inform. 2022;21:11769351221110872. doi: 10.1177/11769351221110872
  • Kobayashi ES, Batalov S, Wenger AM, et al. Approaches to long-read sequencing in a clinical setting to improve diagnostic rate. Sci Rep. 2022;12(1):16945. doi: 10.1038/s41598-022-20113-x
  • Richards S, Aziz N, Bale S, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American college of medical genetics and genomics and the association for molecular pathology. Genet Med. 2015;17(5):405–424. doi: 10.1038/gim.2015.30
  • Gordon AS, Fulton RS, Qin X, et al. Pgrnseq: a targeted capture sequencing panel for pharmacogenetic research and implementation. Pharmacogenet Genom. 2016;26(4):161–168. doi: 10.1097/FPC.0000000000000202
  • Lee S, Shin J-Y, Kwon N-J, et al. ClinPharmSeq: A targeted sequencing panel for clinical pharmacogenetics implementation. PloS One. 2022;17(7):e0272129. doi: 10.1371/journal.pone.0272129
  • Gulilat M, Lamb T, Teft WA, et al. Targeted next generation sequencing as a tool for precision medicine. BMC Med Genomics. 2019;12(1):81. doi: 10.1186/s12920-019-0527-2
  • Fukunaga K, Momozawa Y, Mushiroda T. Update on next generation sequencing of pharmacokinetics-related genes: development of the PKseq panel, a platform for amplicon sequencing of drug-metabolizing enzyme and drug transporter genes. Drug Metab Pharmacokinet. 2021;37:100370. doi: 10.1016/j.dmpk.2020.11.005
  • Han SM, Park J, Lee JH, et al. Targeted next-generation sequencing for comprehensive genetic profiling of pharmacogenes. Clin Pharmacol Ther. 2017;101(3):396–405. doi: 10.1002/cpt.532
  • Klein K, Tremmel R, Winter S, et al. A new panel-based next-generation sequencing method for ADME genes reveals novel associations of common and rare variants with expression in a human liver cohort. Front Genet. 2019;10:7. doi: 10.3389/fgene.2019.00007
  • Yang Y, Muzny DM, Reid JG, et al. Clinical whole-exome sequencing for the diagnosis of mendelian disorders. N Engl J Med. 2013;369:1502–1511. doi: 10.1056/NEJMoa1306555
  • Stavropoulos DJ, Merico D, Jobling R, et al. Whole-genome sequencing expands diagnostic utility and improves clinical management in paediatric medicine. NPJ Genom Med. 2016;1(1):15012. doi: 10.1038/npjgenmed.2015.12
  • Lanillos J, Carcajona M, Maietta P, et al. Clinical pharmacogenetic analysis in 5,001 individuals with diagnostic exome sequencing data. NPJ Genom Med. 2022;7(1):12. doi: 10.1038/s41525-022-00283-3
  • van der Lee M, Allard WG, Bollen S, et al. Repurposing of diagnostic whole exome sequencing data of 1,583 individuals for clinical pharmacogenetics. Clin Pharmacol Ther. 2020;107(3):617–627. doi: 10.1002/cpt.1665
  • Yu MHC, Chan MCY, Chung CCY, et al. Actionable pharmacogenetic variants in Hong Kong Chinese exome sequencing data and projected prescription impact in the Hong Kong population. PloS Genet. 2021;17:e1009323. doi: 10.1371/journal.pgen.1009323
  • Cousin MA, Matey ET, Blackburn PR, et al. Pharmacogenomic findings from clinical whole exome sequencing of diagnostic odyssey patients. Mol Genet Genomic Med. 2017;5(3):269–279. doi: 10.1002/mgg3.283
  • Nishimura AA, Shirts BH, Dorschner MO, et al. Development of clinical decision support alerts for pharmacogenomic incidental findings from exome sequencing. Genet Med. 2015;17(11):939–942. doi: 10.1038/gim.2015.5
  • Caspar SM, Schneider T, Meienberg J, et al. Added value of clinical sequencing: WGS-Based profiling of pharmacogenes. Int J Mol Sci. 2020;21(7):2308. doi: 10.3390/ijms21072308
  • Cohn I, Paton TA, Marshall CR, et al. Genome sequencing as a platform for pharmacogenetic genotyping: a pediatric cohort study. NPJ Genom Med. 2017;2(1):19. doi: 10.1038/s41525-017-0021-8
  • Pan A, Scodellaro S, Khan T, et al. Pharmacogenetic profiling via genome sequencing in children with medical complexity. Pediatr Res. 2023;93(4):905–910. doi: 10.1038/s41390-022-02313-3
  • Mosele F, Remon J, Mateo J, et al. Recommendations for the use of next-generation sequencing (NGS) for patients with metastatic cancers: a report from the ESMO precision medicine working group. Ann Oncol. 2020;31(11):1491–1505. doi: 10.1016/j.annonc.2020.07.014
  • Samsom K, Monkhorst K, Luuk J, et al. Feasibility of whole-genome sequencing in routine clinical practice. J Clin Oncol. 2021;39(15_suppl):3013. doi: 10.1200/JCO.2021.39.15_suppl.3013
  • Weiss JR, Baer MR, Ambrosone CB, et al. Concordance of pharmacogenetic polymorphisms in tumor and germ line DNA in adult patients with acute myeloid leukemia. Cancer Epidemiol Biomarkers Prev. 2007;16(5):1038–1041. doi: 10.1158/1055-9965.EPI-06-0964
  • Hertz DL, Kidwell KM, Thibert JN, et al. Genotyping concordance in DNA extracted from formalin‐fixed paraffin embedded (FFPE) breast tumor and whole blood for pharmacogenetic analyses. Mol Oncol. 2015;9(9):1868–1876. doi: 10.1016/j.molonc.2015.07.002
  • Gillis N, Etheridge AS, Patil SA, et al. Sequencing of genes of drug response in tumor DNA and implications for precision medicine in cancer patients. Pharmacogenomics J. 2023;23(4):73–81. doi: 10.1038/s41397-023-00299-7
  • Mandelker D, Ceyhan-Birsoy O. Evolving significance of tumor-normal sequencing in cancer care. Trends Cancer. 2020;6(1):31–39. doi: 10.1016/j.trecan.2019.11.006
  • Henson JW. Paired tumor-germline testing as a driver in better cancer care. JAMA Netw Open. 2022;5(5):e2213077. doi: 10.1001/jamanetworkopen.2022.13077
  • Hertz DL, Glatz A, Pasternak AL, et al. Integration of germline pharmacogenetics into a tumor sequencing program. JCO Precis Oncol. 2018;2(2):1–15. doi: 10.1200/PO.18.00011
  • Janssens ACJW, Evans JP. Returning pharmacogenetic secondary findings from genome sequencing: let’s not put the cart before the horse. Genet Med. 2015;17(11):854–856. doi: 10.1038/gim.2015.59
  • Lee S, Wheeler MM, Patterson K, et al. Stargazer: a software tool for calling star alleles from next-generation sequencing data using CYP2D6 as a model. Genet Med. 2019;21(2):361–372. doi: 10.1038/s41436-018-0054-0
  • Hari A, Zhou Q, Gonzaludo N, et al. An efficient genotyper and star-allele caller for pharmacogenomics. Genome Res. 2023;33(1):61–70. doi: 10.1101/gr.277075.122
  • Sangkuhl K, Whirl-Carrillo M, Whaley RM, et al. Pharmacogenomics clinical annotation tool (PharmCAT). Clin Pharmacol Ther. 2020;107(1):203–210. doi: 10.1002/cpt.1568
  • Klanderman BJ, Koch C, Machini K, et al. Automated pharmacogenomic reports for clinical genome sequencing. J Mol Diagn. 2022;24(3):205–218. doi: 10.1016/j.jmoldx.2021.12.001
  • Coppola L, Cianflone A, Grimaldi AM, et al. Biobanking in health care: evolution and future directions. J Transl Med. 2019;17(1):172. doi: 10.1186/s12967-019-1922-3
  • Halldorsson BV, Eggertsson HP, Moore KHS, et al. The sequences of 150,119 genomes in the UK biobank. Nature. 2022;607(7920):732–740. doi: 10.1038/s41586-022-04965-x
  • Leitsalu L, Alavere H, Tammesoo M-L, et al. Linking a population biobank with national health registries—the Estonian experience. J Pers Med. 2015;5(2):96–106. doi: 10.3390/jpm5020096
  • Zhou Y, Ingelman‐Sundberg M, Lauschke V. Worldwide distribution of cytochrome P450 alleles: a meta‐analysis of population‐scale sequencing projects. Clin Pharmacol Ther. 2017;102(4):688–700. doi: 10.1002/cpt.690
  • Santos M, Niemi M, Hiratsuka M, et al. Novel copy-number variations in pharmacogenes contribute to interindividual differences in drug pharmacokinetics. Genet Med. 2018;20(6):622–629. doi: 10.1038/gim.2017.156
  • Zhou Y, Lauschke VM. The genetic landscape of major drug metabolizing cytochrome P450 genes—an updated analysis of population-scale sequencing data. Pharmacogenomics J. 2022;22(5–6):284–293. doi: 10.1038/s41397-022-00288-2
  • Hauser AS, Chavali S, Masuho I, et al. Pharmacogenomics of GPCR drug targets. Cell. 2018;172(1–2):41–54. doi: 10.1016/j.cell.2017.11.033
  • Xiao Q, Zhou Y, Winter S, et al. Germline variant burden in multidrug resistance transporters is a therapy‐specific predictor of survival in breast cancer patients. Int J Cancer. 2020;146(9):2475–2487. doi: 10.1002/ijc.32898
  • Ji Y, Skierka JM, Blommel JH, et al. Preemptive pharmacogenomic testing for precision medicine a comprehensive analysis of five actionable pharmacogenomic genes using next-generation DNA sequencing and a customized CYP2D6 genotyping cascade. J Mol Diagn. 2016;18(3):438–445. doi: 10.1016/j.jmoldx.2016.01.003
  • Devarajan S, Moon I, Ho M, et al. Pharmacogenomic next-generation DNA sequencing: lessons from the identification and functional characterization of variants of unknown significance in CYP2C9 and CYP2C19. Drug Metab Dispos. 2019;47(4):425–435. doi: 10.1124/dmd.118.084269
  • Wang L, Scherer SE, Bielinski SJ, et al. Implementation of preemptive DNA sequence–based pharmacogenomics testing across a large academic medical center: the mayo-baylor RIGHT 10K study. Genet Med. 2022;24(5):1062–1072. doi: 10.1016/j.gim.2022.01.022
  • Tafazoli A, van der Lee M, Swen JJ, et al. Development of an extensive workflow for comprehensive clinical pharmacogenomic profiling: lessons from a pilot study on 100 whole exome sequencing data. Pharmacogenomics J. 2022;22(5–6):276–283. doi: 10.1038/s41397-022-00286-4
  • Gaedigk A, Boone EC, Scherer SE, et al. CYP2C8, CYP2C9, and CYP2C19 characterization using next-generation sequencing and haplotype analysis a GeT-RM collaborative project. J Mol Diagn. 2022;24(4):337–350. doi: 10.1016/j.jmoldx.2021.12.011
  • Siamoglou S, Koromina M, Hishinuma E, et al. Identification and functional validation of novel pharmacogenomic variants using a next-generation sequencing-based approach for clinical pharmacogenomics. Pharmacol Res. 2022;176:106087. doi: 10.1016/j.phrs.2022.106087
  • Ly RC, Schmidt RE, Kiel PJ, et al. Severe capecitabine toxicity associated with a rare DPYD variant identified through whole-genome sequencing. JCO Precis Oncol. 2020;4(4):632–638. doi: 10.1200/PO.20.00067
  • DeMattia E, Silvestri M, Polesel J, et al. Rare genetic variant burden in DPYD predicts severe fluoropyrimidine-related toxicity risk. Biomed Pharmacother. 2022;154:113644. doi: 10.1016/j.biopha.2022.113644
  • Mak ACY, White MJ, Eckalbar WL, et al. Whole-genome sequencing of pharmacogenetic drug response in racially diverse children with asthma. Am J Respir Crit Care Med. 2018;197(12):1552–1564. doi: 10.1164/rccm.201712-2529OC
  • van der Lee M, Allard WG, Vossen RHAM, et al. Toward predicting CYP2D6-mediated variable drug response from CYP2D6 gene sequencing data. Sci Transl Med. 2021;13(603):eabf3637. doi: 10.1126/scitranslmed.abf3637
  • Cruz-Correa OF, Len-Cachn RBR, Barrera-Saldaa HA, et al. Prediction of atorvastatin plasmatic concentrations in healthy volunteers using integrated pharmacogenetics sequencing. Pharmacogenomics. 2017;18(2):121–131. doi: 10.2217/pgs-2016-0072
  • Ramsey LB, Bruun GH, Yang W, et al. Rare versus common variants in pharmacogenetics: SLCO1B1 variation and methotrexate disposition. Genome Res. 2012;22(1):1–8. doi: 10.1101/gr.129668.111
  • Mizzi C, Peters B, Mitropoulou C, et al. Personalized pharmacogenomics profiling using whole-genome sequencing. Pharmacogenomics. 2014;15(9):1223–1234. doi: 10.2217/pgs.14.102
  • Bielinski SJ, Sauver JLS, Olson JE, et al. Cohort profile: the right drug, right dose, right time: using genomic data to individualize treatment protocol (RIGHT protocol). Int J Epidemiol. 2019;49(1):23–24k. doi: 10.1093/ije/dyz123
  • Shrestha S, Zhang C, Jerde CR, et al. Gene-specific variant classifier (DPYD-Varifier) to identify deleterious alleles of dihydropyrimidine dehydrogenase. Clin Pharmacol Ther. 2018;104(4):709–718. doi: 10.1002/cpt.1020
  • Lam YWF. Scientific challenges and implementation barriers to translation of pharmacogenomics in clinical practice. ISRN Pharmacol. 2013;2013:641089. doi: 10.1155/2013/641089
  • Manolio TA, Chisholm RL, Ozenberger B, et al. Implementing genomic medicine in the clinic: the future is here. Genet Med. 2013;15(4):258–267. doi: 10.1038/gim.2012.157
  • Qureshi S, Latif A, Condon L, et al. Understanding the barriers and enablers of pharmacogenomic testing in primary care: a qualitative systematic review with meta-aggregation synthesis. Pharmacogenomics. 2021;23(2):135–154. doi: 10.2217/pgs-2021-0131
  • Russell LE, Zhou Y, Almousa AA, et al. Pharmacogenomics in the era of next generation sequencing – from byte to bedside. Drug Metab Rev. 2021;53(2):253–278. doi: 10.1080/03602532.2021.1909613
  • Chen J, Madireddi S, Nagarkar D, et al. In silico tools for accurate HLA and KIR inference from clinical sequencing data empower immunogenetics on individual-patient and population scales. Brief Bioinform. 2021;22(3):bbaa223. doi: 10.1093/bib/bbaa223
  • Chen X, Shen F, Gonzaludo N, et al. Cyrius: accurate CYP2D6 genotyping using whole-genome sequencing data. Pharmacogenomics J. 2021;21(2):251–261. doi: 10.1038/s41397-020-00205-5
  • van der Lee M, Kriek M, Guchelaar H-J, et al. Technologies for pharmacogenomics: a review. Genes. 2020;11:1456. doi: 10.3390/genes11121456
  • Verbelen M, Weale ME, Lewis CM. Cost-effectiveness of pharmacogenetic-guided treatment: are we there yet? Pharmacogenomics J. 2017;17(5):395–402. doi: 10.1038/tpj.2017.21
  • Zhu Y, Swanson KM, Rojas RL, et al. Systematic review of the evidence on the cost-effectiveness of pharmacogenomics-guided treatment for cardiovascular diseases. Genet Med. 2020;22(3):475–486. doi: 10.1038/s41436-019-0667-y
  • Ghanbarian S, Wong GWK, Bunka M, et al. Cost-effectiveness of pharmacogenomic-guided treatment for major depression. CMAJ. 2023;195(44):E1499–E1508. doi: 10.1503/cmaj.221785
  • Muir P, Li S, Lou S, et al. The real cost of sequencing: scaling computation to keep pace with data generation. Genome Biol. 2016;17(1):53. doi: 10.1186/s13059-016-0917-0
  • Krumm N, Hoffman N. Practical estimation of cloud storage costs for clinical genomic data. Pract Lab Med. 2020;21:e00168. doi: 10.1016/j.plabm.2020.e00168
  • Weymann D, Laskin J, Roscoe R, et al. The cost and cost trajectory of whole‐genome analysis guiding treatment of patients with advanced cancers. Mol Genet Genomic Med. 2017;5(3):251–260. doi: 10.1002/mgg3.281
  • Lemke LK, Alam B, Williams R, et al. Reimbursement of pharmacogenetic tests at a tertiary academic medical center in the United States. Front Pharmacol. 2023;14:1179364. doi: 10.3389/fphar.2023.1179364
  • Vozikis A, Cooper DN, Mitropoulou C, et al. Test pricing and reimbursement in genomic medicine: towards a general strategy. Public Health Genomics. 2016;19(6):352–363. doi: 10.1159/000449152