Large-Scale Pharmacogenomics Analysis of Patients With Cancer Within the 100,000 Genomes Project Combining Whole-Genome Sequencing and Medical Records to Inform Clinical Practice

I Ivone U.S. Leong (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) C Claudia P. Cabrera (Clinical Pharmacology and Precision Medicine, William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom) V Valentina Cipriani P Paul J. Ross (Guy's & St Thomas' NHS Foundation Trust, London, United Kingdom) R Richard M. Turner (Wolfson Centre for Personalised Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom) A Alex Stuckey (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) S Sonali Sanghvi (Integrating Pharmacy & Medicines Optimisation Team, NHS North Central London Integrated Care System, UCLH NHS Foundation Trust, London) D Dorota Pasko (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) L Loukas Moutsianas C Christopher A. Odhams (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) G Greg S. Elgar (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) G Georgia Chan (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) A Adam Giess (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) S Susan Walker R Rebecca E. Foulger (SciBite Limited, BioData Innovation Centre, Wellcome Genome Campus, Hinxton, UK) E Eleanor M. Williams (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) L Louise C. Daugherty (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) A Antonio Rueda-Martin (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) D Daniel J. Rhodes (BenevolentAI, London, United Kingdom) O Olivia Niblock (Cambridge Genomics Laboratory, United Kingdom) A Alexandra Pickard (NHS England and NHS Improvement, London, United Kingdom) L Lauren Marks (NHS England and NHS Improvement, London, United Kingdom) S Sarah E.A. Leigh (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) M Matthew J. Welland (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) M Marta Bleda (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) C Catherine Snow (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) Z Zandra Deans (NHS England and NHS Improvement, London, United Kingdom) N Nirupa Murugaesu (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) R Richard H. Scott (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) M Michael R. Barnes M Matthew A. Brown A Augusto Rendon (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) S Sue Hill (NHS England and NHS Improvement, London, United Kingdom) A Alona Sosinsky (Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom) M Mark J. Caulfield (Clinical Pharmacology and Precision Medicine, William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom) E Ellen M. McDonagh

Abstract

PURPOSE As part of the 100,000 Genomes Project, we set out to assess the potential viability and clinical impact of reporting genetic variants associated with drug-induced toxicity for patients with cancer recruited for whole-genome sequencing (WGS) as part of a genomic medicine service. METHODS Germline WGS from 76,805 participants was analyzed for pharmacogenetic (PGx) variants in four genes ( DPYD , NUDT15 , TPMT , UGT1A1 ) associated with toxicity induced by five drugs used in cancer treatment (capecitabine, fluorouracil, mercaptopurine, thioguanine, irinotecan). Linking genomic data with prescribing and hospital incidence records, a phenome-wide association study (PheWAS) was performed to identify whether phenotypes indicative of adverse drug reactions (ADRs) were enriched in drug-exposed individuals with the relevant PGx variants. In a subset of 7,081 patients with cancer, DPYD variants were reported back to clinicians and outcomes were collected. RESULTS We identified clinically relevant PGx variants across the four genes in 62.7% of participants in our cohort. Extending this to annual prescription numbers in England for the drugs affected by these PGx variants, approximately 14,540 patients per year could potentially benefit from a reduced dose or alternative drug to reduce the risk of ADRs. Validating PGx associations in a real-world data set, we found a significant association between PGx variants in DPYD and toxicity-related phenotypes in patients treated with capecitabine or fluorouracil. Reported DPYD variants were deemed informative for clinical decision making in a majority of cases. CONCLUSION Reporting PGx variants from germline WGS relevant to patients with cancer alongside primary findings related to their cancer can be clinically informative, informing prescribing to reduce the risk of ADRs. Extending the range of actionable variants to those found in patients of non-European ancestry is important and will extend the potential clinical impact.

Article Details

Volume / Issue Vol. 43, Issue 6
Published February 20, 2025
Pages 682-693
ISSN 0732-183X
Publisher Lippincott Williams & Wilkins

Journal Info

Journal of Clinical Oncology

Lippincott Williams & Wilkins

ISSN: 0732-183X Health Sciences

Authors (36)

I

Ivone U.S. Leong

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

C

Claudia P. Cabrera

Clinical Pharmacology and Precision Medicine, William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom

V

Valentina Cipriani

P

Paul J. Ross

Guy's & St Thomas' NHS Foundation Trust, London, United Kingdom

R

Richard M. Turner

Wolfson Centre for Personalised Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom

A

Alex Stuckey

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

S

Sonali Sanghvi

Integrating Pharmacy & Medicines Optimisation Team, NHS North Central London Integrated Care System, UCLH NHS Foundation Trust, London

D

Dorota Pasko

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

L

Loukas Moutsianas

C

Christopher A. Odhams

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

G

Greg S. Elgar

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

G

Georgia Chan

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

A

Adam Giess

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

S

Susan Walker

R

Rebecca E. Foulger

SciBite Limited, BioData Innovation Centre, Wellcome Genome Campus, Hinxton, UK

E

Eleanor M. Williams

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

L

Louise C. Daugherty

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

A

Antonio Rueda-Martin

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

D

Daniel J. Rhodes

BenevolentAI, London, United Kingdom

O

Olivia Niblock

Cambridge Genomics Laboratory, United Kingdom

A

Alexandra Pickard

NHS England and NHS Improvement, London, United Kingdom

L

Lauren Marks

NHS England and NHS Improvement, London, United Kingdom

S

Sarah E.A. Leigh

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

M

Matthew J. Welland

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

M

Marta Bleda

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

C

Catherine Snow

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

Z

Zandra Deans

NHS England and NHS Improvement, London, United Kingdom

N

Nirupa Murugaesu

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

R

Richard H. Scott

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

M

Michael R. Barnes

M

Matthew A. Brown

A

Augusto Rendon

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

S

Sue Hill

NHS England and NHS Improvement, London, United Kingdom

A

Alona Sosinsky

Genomics England Ltd, Level 21 One Canada Square, London, United Kingdom

M

Mark J. Caulfield

Clinical Pharmacology and Precision Medicine, William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, United Kingdom

E

Ellen M. McDonagh