Large-scale meta-genome-wide association study reveals common genetic factors linked to radiation-induced acute toxicities across cancer types.


Journal

JNCI cancer spectrum
ISSN: 2515-5091
Titre abrégé: JNCI Cancer Spectr
Pays: England
ID NLM: 101721827

Informations de publication

Date de publication:
31 Oct 2023
Historique:
received: 07 06 2023
revised: 18 09 2023
accepted: 18 10 2023
medline: 27 11 2023
pubmed: 20 10 2023
entrez: 20 10 2023
Statut: ppublish

Résumé

This study was designed to identify common genetic susceptibility and shared genetic variants associated with acute radiation-induced toxicity across 4 cancer types (prostate, head and neck, breast, and lung). A genome-wide association study meta-analysis was performed using 19 cohorts totaling 12 042 patients. Acute standardized total average toxicity (STATacute) was modelled using a generalized linear regression model for additive effect of genetic variants, adjusted for demographic and clinical covariates (rSTATacute). Linkage disequilibrium score regression estimated shared single-nucleotide variation (SNV-formerly SNP)-based heritability of rSTATacute in all patients and for each cancer type. Shared SNV-based heritability of STATacute among all cancer types was estimated at 10% (SE = 0.02) and was higher for prostate (17%, SE = 0.07), head and neck (27%, SE = 0.09), and breast (16%, SE = 0.09) cancers. We identified 130 suggestive associated SNVs with rSTATacute (5.0 × 10‒8 < P < 1.0 × 10‒5) across 25 genomic regions. rs142667902 showed the strongest association (effect allele A; effect size ‒0.17; P = 1.7 × 10‒7), which is located near DPPA4, encoding a protein involved in pluripotency in stem cells, which are essential for repair of radiation-induced tissue injury. Gene-set enrichment analysis identified 'RNA splicing via endonucleolytic cleavage and ligation' (P = 5.1 × 10‒6, P = .079 corrected) as the top gene set associated with rSTATacute among all patients. In silico gene expression analysis showed that the genes associated with rSTATacute were statistically significantly up-regulated in skin (not sun exposed P = .004 corrected; sun exposed P = .026 corrected). There is shared SNV-based heritability for acute radiation-induced toxicity across and within individual cancer sites. Future meta-genome-wide association studies among large radiation therapy patient cohorts are worthwhile to identify the common causal variants for acute radiotoxicity across cancer types.

Sections du résumé

BACKGROUND BACKGROUND
This study was designed to identify common genetic susceptibility and shared genetic variants associated with acute radiation-induced toxicity across 4 cancer types (prostate, head and neck, breast, and lung).
METHODS METHODS
A genome-wide association study meta-analysis was performed using 19 cohorts totaling 12 042 patients. Acute standardized total average toxicity (STATacute) was modelled using a generalized linear regression model for additive effect of genetic variants, adjusted for demographic and clinical covariates (rSTATacute). Linkage disequilibrium score regression estimated shared single-nucleotide variation (SNV-formerly SNP)-based heritability of rSTATacute in all patients and for each cancer type.
RESULTS RESULTS
Shared SNV-based heritability of STATacute among all cancer types was estimated at 10% (SE = 0.02) and was higher for prostate (17%, SE = 0.07), head and neck (27%, SE = 0.09), and breast (16%, SE = 0.09) cancers. We identified 130 suggestive associated SNVs with rSTATacute (5.0 × 10‒8 < P < 1.0 × 10‒5) across 25 genomic regions. rs142667902 showed the strongest association (effect allele A; effect size ‒0.17; P = 1.7 × 10‒7), which is located near DPPA4, encoding a protein involved in pluripotency in stem cells, which are essential for repair of radiation-induced tissue injury. Gene-set enrichment analysis identified 'RNA splicing via endonucleolytic cleavage and ligation' (P = 5.1 × 10‒6, P = .079 corrected) as the top gene set associated with rSTATacute among all patients. In silico gene expression analysis showed that the genes associated with rSTATacute were statistically significantly up-regulated in skin (not sun exposed P = .004 corrected; sun exposed P = .026 corrected).
CONCLUSIONS CONCLUSIONS
There is shared SNV-based heritability for acute radiation-induced toxicity across and within individual cancer sites. Future meta-genome-wide association studies among large radiation therapy patient cohorts are worthwhile to identify the common causal variants for acute radiotoxicity across cancer types.

Identifiants

pubmed: 37862240
pii: 7325356
doi: 10.1093/jncics/pkad088
pmc: PMC10653584
pii:
doi:

Types de publication

Meta-Analysis Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Cancer Research UK
Pays : United Kingdom

Investigateurs

Elnaz Naderi (E)
Miguel E Aguado-Barrera (ME)
Line M H Schack (LMH)
Leila Dorling (L)
Tim Rattay (T)
Laura Fachal (L)
Holly Summersgill (H)
Laura Martínez-Calvo (L)
Ceilidh Welsh (C)
Tom Dudding (T)
Yasmin Odding (Y)
Ana Varela-Pazos (A)
Rajesh Jena (R)
David J Thomson (DJ)
Roel J H M Steenbakkers (RJHM)
Joe Dennis (J)
Ramón Lobato-Busto (R)
Jan Alsner (J)
Andy Ness (A)
Chris Nutting (C)
Antonio Gómez-Caamaño (A)
Jesper G Eriksen (JG)
Steve J Thomas (SJ)
Amy M Bates (AM)
Adam J Webb (AJ)
Ananya Choudhury (A)
Barry S Rosenstein (BS)
Begona Taboada-Valladares (B)
Carsten Herskind (C)
David Azria (D)
David P Dearnaley (DP)
Dirk de Ruysscher (D)
Elena Sperk (E)
Emma Hall (E)
Hilary Stobart (H)
Jenny Chang-Claude (J)
Kim De Ruyck (K)
Liv Veldeman (L)
Manuel Altabas (M)
Maria Carmen De Santis (MC)
Marie-Pierre Farcy-Jacquet (MP)
Marlon R Veldwijk (MR)
Matthew R Sydes (MR)
Matthew Parliament (M)
Nawaid Usmani (N)
Neil G Burnet (NG)
Petra Seibold (P)
R Paul Symonds (RP)
Rebecca M Elliott (RM)
Renée Bultijnck (R)
Sara Gutiérrez-Enríquez (S)
Meritxell Mollà (M)
Sarah L Gulliford (SL)
Sheryl Green (S)
Tiziana Rancati (T)
Victoria Reyes (V)
Ana Carballo (A)
Paula Peleteiro (P)
Paloma Sosa-Fajardo (P)
Chris Parker (C)
Valérie Fonteyne (V)
Kerstie Johnson (K)
Maarten Lambrecht (M)
Ben Vanneste (B)
Riccardo Valdagni (R)
Alexandra Giraldo (A)
Mónica Ramos (M)
Brenda Diergaarde (B)
Geoffrey Liu (G)
Suzanne M Leal (SM)
Melvin L K Chua (MLK)
Miranda Pring (M)
Jens Overgaard (J)
Luis M Cascallar-Caneda (LM)
Fréderic Duprez (F)
Christopher J Talbot (CJ)
Gillian C Barnett (GC)
Alison M Dunning (AM)
Ana Vega (A)
Christian Nicolaj Andreassen (CN)
Johannes A Langendijk (JA)
Catharine M L West (CML)
Behrooz Z Alizadeh (BZ)
Sarah L Kerns (SL)

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press.

Références

Stem Cells. 2007 Jan;25(1):19-28
pubmed: 16990585
Am J Hum Genet. 2017 Jul 6;101(1):5-22
pubmed: 28686856
PLoS Comput Biol. 2015 Apr 17;11(4):e1004219
pubmed: 25885710
Carcinogenesis. 2015 Mar;36(3):307-17
pubmed: 25604391
Nat Genet. 2019 Mar;51(3):431-444
pubmed: 30804558
Nucleus. 2016 Apr 25;7(2):138-45
pubmed: 27310306
Nat Genet. 2014 Aug;46(8):891-4
pubmed: 24974847
J Transl Med. 2021 Nov 27;19(1):481
pubmed: 34838041
Radiother Oncol. 2022 Nov;176:138-148
pubmed: 36191651
Nat Genet. 2013 Jun;45(6):580-5
pubmed: 23715323
Nat Commun. 2017 Nov 28;8(1):1826
pubmed: 29184056
Bioinformatics. 2010 Sep 1;26(17):2190-1
pubmed: 20616382
Nat Genet. 2018 May;50(5):737-745
pubmed: 29700474
Am J Hum Genet. 2007 Sep;81(3):559-75
pubmed: 17701901
Nat Immunol. 2008 May;9(5):503-10
pubmed: 18425107
Front Genet. 2020 Dec 03;11:592461
pubmed: 33343632
Radiother Oncol. 2013 Jun;107(3):295-9
pubmed: 23618501
Nat Genet. 2015 Mar;47(3):291-5
pubmed: 25642630
Nat Genet. 2015 Nov;47(11):1236-41
pubmed: 26414676
Clin Exp Pharmacol Physiol. 2005 Jul;32(7):503-14
pubmed: 16026507
Radiother Oncol. 2002 Aug;64(2):131-40
pubmed: 12242122
Nature. 2014 Jul 24;511(7510):421-7
pubmed: 25056061
Radiother Oncol. 2014 May;111(2):178-85
pubmed: 24785509
Biomolecules. 2015 Oct 29;5(4):2935-77
pubmed: 26529031
Nat Genet. 2021 Mar;53(3):413
pubmed: 33473200
Int J Cancer. 1999 Jan 18;80(2):279-84
pubmed: 9935211
J Pharm Biomed Anal. 2016 Jan 25;118:380-386
pubmed: 26609677
Oncotarget. 2018 Mar 30;9(24):17078-17092
pubmed: 29682206
Mol Cancer Res. 2020 Dec;18(12):1839-1848
pubmed: 32928910
Nat Genet. 2017 Aug 30;49(9):1304-1310
pubmed: 28854176
Int J Radiat Oncol Biol Phys. 2009 Mar 15;73(4):1187-95
pubmed: 19251090
J Urol. 2014 Aug;192(2):575-82
pubmed: 24518784
EBioMedicine. 2016 Aug;10:150-63
pubmed: 27515689
Br J Cancer. 2022 Apr;126(7):1082-1090
pubmed: 35039627
Semin Radiat Oncol. 1994 Apr;4(2):68-80
pubmed: 10717093
J Transl Med. 2022 Aug 12;20(1):360
pubmed: 35962345
Nat Genet. 2007 Jul;39(7):906-13
pubmed: 17572673
J Natl Cancer Inst. 2020 Feb 1;112(2):179-190
pubmed: 31095341
Radiat Res. 2019 Jan;191(1):93-106
pubmed: 30407899
Bioinformatics. 2021 Apr 9;37(1):129-130
pubmed: 33416854
Int J Med Sci. 2012;9(3):193-9
pubmed: 22408567
Int J Radiat Oncol Biol Phys. 2012 Mar 1;82(3):1065-74
pubmed: 21605943

Auteurs

Elnaz Naderi (E)

Department of Epidemiology, University Medical Center Groningen, Groningen, The Netherlands.
Department of Radiation Oncology, University Medical Center Groningen, Groningen, The Netherlands.
Center for Statistical Genetics, Gertrude H. Sergievsky Center, and the Department of Neurology, Columbia University Medical Center, New York, NY, USA.

Miguel E Aguado-Barrera (ME)

Fundación Pública Galega Medicina Xenómica, Santiago de Compostela, Spain.
Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.

Line M H Schack (LMH)

Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus, Denmark.
Department of Oncology, Gødstrup Hospital, Herning, Denmark.
NIDO | Centre for Research and Education, Gødstrup Hospital, Herning, Denmark.

Leila Dorling (L)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.

Tim Rattay (T)

Leicester Cancer Research Centre, University of Leicester, Leicester, UK.

Laura Fachal (L)

Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, UK.
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.

Holly Summersgill (H)

Manchester Academic Health Science Centre, The Christie NHS Foundation Trust, Manchester, UK.

Laura Martínez-Calvo (L)

Fundación Pública Galega Medicina Xenómica, Santiago de Compostela, Spain.
Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.

Ceilidh Welsh (C)

Department of Oncology, University of Cambridge, Cambridge, UK.

Tom Dudding (T)

Bristol Dental School, University of Bristol, Bristol, UK.
MRC Integrative Epidemiology Unit, University of Bristol, Bristol, UK.

Yasmin Odding (Y)

Bristol Cancer Institute, University Hospitals Bristol NHS Foundation Trust, Bristol, UK.

Ana Varela-Pazos (A)

Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Rajesh Jena (R)

Department of Oncology, Addenbrooke's Hospital, University of Cambridge, Cambridge, UK.

David J Thomson (DJ)

Division of Cancer Sciences, University of Manchester, Manchester, UK.
The Christie NHS Foundation Trust, Manchester, UK.

Roel J H M Steenbakkers (RJHM)

Department of Radiation Oncology, University Medical Center Groningen, Groningen, The Netherlands.

Joe Dennis (J)

Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.

Ramón Lobato-Busto (R)

Department of Medical Physics, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Jan Alsner (J)

Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus, Denmark.

Andy Ness (A)

Bristol Dental School, University of Bristol, Bristol, UK.

Chris Nutting (C)

Head and Neck Unit, The Royal Marsden Hospital, London, UK.

Antonio Gómez-Caamaño (A)

Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Jesper G Eriksen (JG)

Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus, Denmark.

Steve J Thomas (SJ)

Bristol Dental School, University of Bristol, Bristol, UK.

Amy M Bates (AM)

Department of Oncology, University of Cambridge, Cambridge, UK.

Adam J Webb (AJ)

Department of Genetics and Genome Biology, University of Leicester, Leicester, UK.

Ananya Choudhury (A)

Division of Cancer Sciences, University of Manchester, Manchester Academic Health Science Centre, Christie Hospital, Manchester, UK.

Barry S Rosenstein (BS)

Department of Radiation Oncology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Begona Taboada-Valladares (B)

Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Carsten Herskind (C)

Department of Radiation Oncology, Universitätsmedizin Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

David Azria (D)

Fédération Universitaire d'Oncologie Radiothérapie d'Occitanie Méditérranée, Département d'Oncologie Radiothérapie, ICM Montpellier, INSERM U1194 IRCM, University of Montpellier, Montpellier, France.

David P Dearnaley (DP)

Division of Radiotherapy and Imaging, The Institute of Cancer Research Department, The Royal Marsden NHS Foundation Trust, London, UK.

Dirk de Ruysscher (D)

MAASTRO Clinic, GROW School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, Netherlands.

Elena Sperk (E)

Department of Radiation Oncology, Universitätsmedizin Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Emma Hall (E)

Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK.

Hilary Stobart (H)

Patient Advocate, Independent Cancer Patients' Voice, London, UK.

Jenny Chang-Claude (J)

Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.
University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Kim De Ruyck (K)

Departments of Basic Medical Sciences and Radiotherapy, Ghent University Hospital, Ghent, Belgium.

Liv Veldeman (L)

Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Department of Radiation Oncology, Ghent University Hospital, Ghent, Belgium.

Manuel Altabas (M)

Radiation Oncology Department, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Spain.

Maria Carmen De Santis (MC)

Radiation Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Marie-Pierre Farcy-Jacquet (MP)

Fédération Universitaire d'Oncologie Radiothérapie d'Occitanie Méditérranée, Département d'Oncologie Radiothérapie, CHU Carémeau, Nîmes, France.

Marlon R Veldwijk (MR)

Department of Radiation Oncology, Universitätsmedizin Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Matthew R Sydes (MR)

MRC Clinical Trials Unit at UCL, Institute of Clinical Trials and Methodology, University College London, London, UK.

Matthew Parliament (M)

Division of Radiation Oncology, Department of Oncology, Cross Cancer Institute, University of Alberta, Edmonton, AB, Canada.

Nawaid Usmani (N)

Division of Radiation Oncology, Department of Oncology, Cross Cancer Institute, University of Alberta, Edmonton, AB, Canada.

Neil G Burnet (NG)

The Christie NHS Foundation Trust, Manchester, UK.

Petra Seibold (P)

Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.

R Paul Symonds (RP)

Cancer Research Centre, University of Leicester, Leicester, UK.

Rebecca M Elliott (RM)

Division of Cancer Sciences, University of Manchester, Manchester Academic Health Science Centre, Christie Hospital, Manchester, UK.

Renée Bultijnck (R)

Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Department of Radiation Oncology, Ghent University Hospital, Ghent, Belgium.

Sara Gutiérrez-Enríquez (S)

Hereditary Cancer Genetics Group, Vall d'Hebron Institute of Oncology, Vall d'Hebron Hospital Campus, Barcelona, Spain.

Meritxell Mollà (M)

Radiation Oncology Department, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Spain.

Sarah L Gulliford (SL)

Department of Medical Physics and Biomedical Engineering, University College London, UK.

Sheryl Green (S)

Department of Radiation Oncology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Tiziana Rancati (T)

Data Science Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Victoria Reyes (V)

Radiation Oncology Department, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Spain.

Ana Carballo (A)

Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Paula Peleteiro (P)

Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Paloma Sosa-Fajardo (P)

Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Chris Parker (C)

Department of Medical Physics and Biomedical Engineering, University College London, UK.

Valérie Fonteyne (V)

Department of Radiation Oncology, Ghent University Hospital, Ghent, Belgium.

Kerstie Johnson (K)

Leicester Cancer Research Centre, University of Leicester, Leicester, UK.

Maarten Lambrecht (M)

Radiation Oncology, KU Leuven, Leuven, Belgium.

Ben Vanneste (B)

Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Department of Radiation Oncology, Ghent University Hospital, Ghent, Belgium.
Department of Radiation Oncology (Maastro Clinic), GROW School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands.

Riccardo Valdagni (R)

Radiation Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
Prostate Cancer Program, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Alexandra Giraldo (A)

Radiation Oncology Department, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Spain.

Mónica Ramos (M)

Radiation Oncology Department, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Spain.

Brenda Diergaarde (B)

Department of Human Genetics, School of Public Health, University of Pittsburgh, UPMC Hillman Cancer Center, Pittsburgh, PA, USA.

Geoffrey Liu (G)

Princess Margaret Cancer Centre, Temerty Faculty of Medicine, Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada.

Suzanne M Leal (SM)

Center for Statistical Genetics, Gertrude H. Sergievsky Center, and the Department of Neurology, Columbia University Medical Center, New York, NY, USA.
Taub Institute for Alzheimer's Disease and the Aging Brain, Columbia University Medical Center, New York, NY, USA.

Melvin L K Chua (MLK)

Division of Radiation Oncology, National Cancer Centre Singapore, Singapore.
Duke-NUS Medical School, Oncology Academic Clinical Programme, Singapore.

Miranda Pring (M)

Bristol Dental School, University of Bristol, Bristol, UK.

Jens Overgaard (J)

Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus, Denmark.

Luis M Cascallar-Caneda (LM)

Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.

Fréderic Duprez (F)

Department of Human Structure and Repair, Ghent University, Ghent, Belgium.
Department of Radiation Oncology, Ghent University Hospital, Ghent, Belgium.

Christopher J Talbot (CJ)

Department of Genetics and Genome Biology, University of Leicester, Leicester, UK.

Gillian C Barnett (GC)

Department of Oncology, Addenbrooke's Hospital, University of Cambridge, Cambridge, UK.

Alison M Dunning (AM)

Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.

Ana Vega (A)

Fundación Pública Galega Medicina Xenómica, Santiago de Compostela, Spain.
Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
Grupo de Medicina Xenómica, Centro de Investigación Biomédica en Red de Enfermedades Raras, Universidade de Santiago de Compostela, Santiago de Compostela, Spain.

Christian Nicolaj Andreassen (CN)

Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus, Denmark.
Department of Oncology, Aarhus University Hospital, Aarhus, Denmark.

Johannes A Langendijk (JA)

Department of Radiation Oncology, University Medical Center Groningen, Groningen, The Netherlands.

Catharine M L West (CML)

Translational Radiobiology Group, Division of Cancer Sciences, University of Manchester, Manchester Academic Health Science Centre, Christie NHS Foundation Trust Hospital, Manchester, UK.

Behrooz Z Alizadeh (BZ)

Department of Epidemiology, University Medical Center Groningen, Groningen, The Netherlands.

Sarah L Kerns (SL)

Department of Radiation Oncology, The Medical College of Wisconsin, Milwaukee, WI, USA.

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