Tumour genomic and microenvironmental heterogeneity for integrated prediction of 5-year biochemical recurrence of prostate cancer: a retrospective cohort study

Summary Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratificatio...

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Published inThe lancet oncology Vol. 15; no. 13; pp. 1521 - 1532
Main Authors Lalonde, Emilie, MSc, Ishkanian, Adrian S, MD, Sykes, Jenna, MMath, Fraser, Michael, PhD, Ross-Adams, Helen, PhD, Erho, Nicholas, MSc, Dunning, Mark J, PhD, Halim, Silvia, MSc, Lamb, Alastair D, FRCS, Moon, Nathalie C, MMath, Zafarana, Gaetano, PhD, Warren, Anne Y, FRCPath, Meng, Xianyue, MSc, Thoms, John, MD, Grzadkowski, Michal R, BMath, Berlin, Alejandro, MD, Have, Cherry L, BSc, Ramnarine, Varune R, BCS, Yao, Cindy Q, MSc, Malloff, Chad A, MSc, Lam, Lucia L, BSc, Xie, Honglei, MMath, Harding, Nicholas J, PhD, Mak, Denise Y F, PhD, Chu, Kenneth C, PhD, Chong, Lauren C, BCS, Sendorek, Dorota H, BSc, P'ng, Christine, BSc, Collins, Colin C, Prof, Squire, Jeremy A, Prof, Jurisica, Igor, Prof, Cooper, Colin, PhD, Eeles, Rosalind, Prof, Pintilie, Melania, MSc, Dal Pra, Alan, MD, Davicioni, Elai, PhD, Lam, Wan L, Prof, Milosevic, Michael, MD, Neal, David E, Prof, van der Kwast, Theodorus, Prof, Boutros, Paul C, Prof, Bristow, Robert G, Prof
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 01.12.2014
Elsevier Limited
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Abstract Summary Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratification and complement clinical prognostic factors. Methods We used DNA-based indices alone or in combination with intra-prostatic hypoxia measurements to develop four prognostic indices in 126 low-risk to intermediate-risk patients (Toronto cohort) who will receive image-guided radiotherapy. We validated these indices in two independent cohorts of 154 (Memorial Sloan Kettering Cancer Center cohort [MSKCC] cohort) and 117 (Cambridge cohort) radical prostatectomy specimens from low-risk to high-risk patients. We applied unsupervised and supervised machine learning techniques to the copy-number profiles of 126 pre-image-guided radiotherapy diagnostic biopsies to develop prognostic signatures. Our primary endpoint was the development of a set of prognostic measures capable of stratifying patients for risk of biochemical relapse 5 years after primary treatment. Findings Biochemical relapse was associated with indices of tumour hypoxia, genomic instability, and genomic subtypes based on multivariate analyses. We identified four genomic subtypes for prostate cancer, which had different 5-year biochemical relapse-free survival. Genomic instability is prognostic for relapse in both image-guided radiotherapy (multivariate analysis hazard ratio [HR] 4·5 [95% CI 2·1–9·8]; p=0·00013; area under the receiver operator curve [AUC] 0·70 [95% CI 0·65–0·76]) and radical prostatectomy (4·0 [1·6–9·7]; p=0·0024; AUC 0·57 [0·52–0·61]) patients with prostate cancer, and its effect is magnified by intratumoral hypoxia (3·8 [1·2–12]; p=0·019; AUC 0·67 [0·61–0·73]). A novel 100-loci DNA signature accurately classified treatment outcome in the MSKCC low-risk to intermediate-risk cohort (multivariate analysis HR 6·1 [95% CI 2·0–19]; p=0·0015; AUC 0·74 [95% CI 0·65–0·83]). In the independent MSKCC and Cambridge cohorts, this signature identified low-risk to high-risk patients who were most likely to fail treatment within 18 months (combined cohorts multivariate analysis HR 2·9 [95% CI 1·4–6·0]; p=0·0039; AUC 0·68 [95% CI 0·63–0·73]), and was better at predicting biochemical relapse than 23 previously published RNA signatures. Interpretation This is the first study of cancer outcome to integrate DNA-based and microenvironment-based failure indices to predict patient outcome. Patients exhibiting these aggressive features after biopsy should be entered into treatment intensification trials. Funding Movember Foundation, Prostate Cancer Canada, Ontario Institute for Cancer Research, Canadian Institute for Health Research, NIHR Cambridge Biomedical Research Centre, The University of Cambridge, Cancer Research UK, Cambridge Cancer Charity, Prostate Cancer UK, Hutchison Whampoa Limited, Terry Fox Research Institute, Princess Margaret Cancer Centre Foundation, PMH-Radiation Medicine Program Academic Enrichment Fund, Motorcycle Ride for Dad (Durham), Canadian Cancer Society.
AbstractList Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30-50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratification and complement clinical prognostic factors. Methods We used DNA-based indices alone or in combination with intra-prostatic hypoxia measurements to develop four prognostic indices in 126 low-risk to intermediate-risk patients (Toronto cohort) who will receive image-guided radiotherapy. We validated these indices in two independent cohorts of 154 (Memorial Sloan Kettering Cancer Center cohort [MSKCC] cohort) and 117 (Cambridge cohort) radical prostatectomy specimens from low-risk to high-risk patients. We applied unsupervised and supervised machine learning techniques to the copy-number profiles of 126 pre-image-guided radiotherapy diagnostic biopsies to develop prognostic signatures. Our primary endpoint was the development of a set of prognostic measures capable of stratifying patients for risk of biochemical relapse 5 years after primary treatment. Findings Biochemical relapse was associated with indices of tumour hypoxia, genomic instability, and genomic subtypes based on multivariate analyses. We identified four genomic subtypes for prostate cancer, which had different 5-year biochemical relapse-free survival. Genomic instability is prognostic for relapse in both image-guided radiotherapy (multivariate analysis hazard ratio [HR] 4.5 [95% CI 2.1-9.8]; p=0.00013; area under the receiver operator curve [AUC] 0.70 [95% CI 0.65-0.76]) and radical prostatectomy (4.0 [1.6-9.7]; p=0.0024; AUC 0.57 [0.52-0.61]) patients with prostate cancer, and its effect is magnified by intratumoral hypoxia (3.8 [1.2-12]; p=0.019; AUC 0.67 [0.61-0.73]). A novel 100-loci DNA signature accurately classified treatment outcome in the MSKCC low-risk to intermediate-risk cohort (multivariate analysis HR 6.1 [95% CI 2.0-19]; p=0.0015; AUC 0.74 [95% CI 0.65-0.83]). In the independent MSKCC and Cambridge cohorts, this signature identified low-risk to high-risk patients who were most likely to fail treatment within 18 months (combined cohorts multivariate analysis HR 2.9 [95% CI 1.4-6.0]; p=0.0039; AUC 0.68 [95% CI 0.63-0.73]), and was better at predicting biochemical relapse than 23 previously published RNA signatures. Interpretation This is the first study of cancer outcome to integrate DNA-based and microenvironment-based failure indices to predict patient outcome. Patients exhibiting these aggressive features after biopsy should be entered into treatment intensification trials. Funding Movember Foundation, Prostate Cancer Canada, Ontario Institute for Cancer Research, Canadian Institute for Health Research, NIHR Cambridge Biomedical Research Centre, The University of Cambridge, Cancer Research UK, Cambridge Cancer Charity, Prostate Cancer UK, Hutchison Whampoa Limited, Terry Fox Research Institute, Princess Margaret Cancer Centre Foundation, PMH-Radiation Medicine Program Academic Enrichment Fund, Motorcycle Ride for Dad (Durham), Canadian Cancer Society.
Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratification and complement clinical prognostic factors. We used DNA-based indices alone or in combination with intra-prostatic hypoxia measurements to develop four prognostic indices in 126 low-risk to intermediate-risk patients (Toronto cohort) who will receive image-guided radiotherapy. We validated these indices in two independent cohorts of 154 (Memorial Sloan Kettering Cancer Center cohort [MSKCC] cohort) and 117 (Cambridge cohort) radical prostatectomy specimens from low-risk to high-risk patients. We applied unsupervised and supervised machine learning techniques to the copy-number profiles of 126 pre-image-guided radiotherapy diagnostic biopsies to develop prognostic signatures. Our primary endpoint was the development of a set of prognostic measures capable of stratifying patients for risk of biochemical relapse 5 years after primary treatment. Biochemical relapse was associated with indices of tumour hypoxia, genomic instability, and genomic subtypes based on multivariate analyses. We identified four genomic subtypes for prostate cancer, which had different 5-year biochemical relapse-free survival. Genomic instability is prognostic for relapse in both image-guided radiotherapy (multivariate analysis hazard ratio [HR] 4·5 [95% CI 2·1–9·8]; p=0·00013; area under the receiver operator curve [AUC] 0·70 [95% CI 0·65–0·76]) and radical prostatectomy (4·0 [1·6–9·7]; p=0·0024; AUC 0·57 [0·52–0·61]) patients with prostate cancer, and its effect is magnified by intratumoral hypoxia (3·8 [1·2–12]; p=0·019; AUC 0·67 [0·61–0·73]). A novel 100-loci DNA signature accurately classified treatment outcome in the MSKCC low-risk to intermediate-risk cohort (multivariate analysis HR 6·1 [95% CI 2·0–19]; p=0·0015; AUC 0·74 [95% CI 0·65–0·83]). In the independent MSKCC and Cambridge cohorts, this signature identified low-risk to high-risk patients who were most likely to fail treatment within 18 months (combined cohorts multivariate analysis HR 2·9 [95% CI 1·4–6·0]; p=0·0039; AUC 0·68 [95% CI 0·63–0·73]), and was better at predicting biochemical relapse than 23 previously published RNA signatures. This is the first study of cancer outcome to integrate DNA-based and microenvironment-based failure indices to predict patient outcome. Patients exhibiting these aggressive features after biopsy should be entered into treatment intensification trials. Movember Foundation, Prostate Cancer Canada, Ontario Institute for Cancer Research, Canadian Institute for Health Research, NIHR Cambridge Biomedical Research Centre, The University of Cambridge, Cancer Research UK, Cambridge Cancer Charity, Prostate Cancer UK, Hutchison Whampoa Limited, Terry Fox Research Institute, Princess Margaret Cancer Centre Foundation, PMH-Radiation Medicine Program Academic Enrichment Fund, Motorcycle Ride for Dad (Durham), Canadian Cancer Society.
Clinical prognostic groupings for localised prostate cancers are imprecise, with 30-50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratification and complement clinical prognostic factors. Methods We used DNA-based indices alone or in combination with intra-prostatic hypoxia measurements to develop four prognostic indices in 126 low-risk to intermediate-risk patients (Toronto cohort) who will receive image-guided radiotherapy. We validated these indices in two independent cohorts of 154 (Memorial Sloan Kettering Cancer Center cohort cohort) and 117 (Cambridge cohort) radical prostatectomy specimens from low-risk to high-risk patients. We applied unsupervised and supervised machine learning techniques to the copy-number profiles of 126 pre-image-guided radiotherapy diagnostic biopsies to develop prognostic signatures. Our primary endpoint was the development of a set of prognostic measures capable of stratifying patients for risk of biochemical relapse 5 years after primary treatment. Findings Biochemical relapse was associated with indices of tumour hypoxia, genomic instability, and genomic subtypes based on multivariate analyses. We identified four genomic subtypes for prostate cancer, which had different 5-year biochemical relapse-free survival. Genomic instability is prognostic for relapse in both image-guided radiotherapy (multivariate analysis hazard ratio 4·5 [95% CI 2·1-9·8]; p=0·00013; area under the receiver operator curve 0·70 [95% CI 0·65-0·76]) and radical prostatectomy (4·0 [1·6-9·7]; p=0·0024; AUC 0·57 [0·52-0·61]) patients with prostate cancer, and its effect is magnified by intratumoral hypoxia (3·8 [1·2-12]; p=0·019; AUC 0·67 [0·61-0·73]). A novel 100-loci DNA signature accurately classified treatment outcome in the MSKCC low-risk to intermediate-risk cohort (multivariate analysis HR 6·1 [95% CI 2·0-19]; p=0·0015; AUC 0·74 [95% CI 0·65-0·83]). In the independent MSKCC and Cambridge cohorts, this signature identified low-risk to high-risk patients who were most likely to fail treatment within 18 months (combined cohorts multivariate analysis HR 2·9 [95% CI 1·4-6·0]; p=0·0039; AUC 0·68 [95% CI 0·63-0·73]), and was better at predicting biochemical relapse than 23 previously published RNA signatures. Interpretation This is the first study of cancer outcome to integrate DNA-based and microenvironment-based failure indices to predict patient outcome. Patients exhibiting these aggressive features after biopsy should be entered into treatment intensification trials. Funding Movember Foundation, Prostate Cancer Canada, Ontario Institute for Cancer Research, Canadian Institute for Health Research, NIHR Cambridge Biomedical Research Centre, The University of Cambridge, Cancer Research UK, Cambridge Cancer Charity, Prostate Cancer UK, Hutchison Whampoa Limited, Terry Fox Research Institute, Princess Margaret Cancer Centre Foundation, PMH-Radiation Medicine Program Academic Enrichment Fund, Motorcycle Ride for Dad (Durham), Canadian Cancer Society.
Summary Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided radiotherapy or radical prostatectomy. We aimed to test combined genomic and microenvironmental indices in prostate cancer to improve risk stratification and complement clinical prognostic factors. Methods We used DNA-based indices alone or in combination with intra-prostatic hypoxia measurements to develop four prognostic indices in 126 low-risk to intermediate-risk patients (Toronto cohort) who will receive image-guided radiotherapy. We validated these indices in two independent cohorts of 154 (Memorial Sloan Kettering Cancer Center cohort [MSKCC] cohort) and 117 (Cambridge cohort) radical prostatectomy specimens from low-risk to high-risk patients. We applied unsupervised and supervised machine learning techniques to the copy-number profiles of 126 pre-image-guided radiotherapy diagnostic biopsies to develop prognostic signatures. Our primary endpoint was the development of a set of prognostic measures capable of stratifying patients for risk of biochemical relapse 5 years after primary treatment. Findings Biochemical relapse was associated with indices of tumour hypoxia, genomic instability, and genomic subtypes based on multivariate analyses. We identified four genomic subtypes for prostate cancer, which had different 5-year biochemical relapse-free survival. Genomic instability is prognostic for relapse in both image-guided radiotherapy (multivariate analysis hazard ratio [HR] 4·5 [95% CI 2·1–9·8]; p=0·00013; area under the receiver operator curve [AUC] 0·70 [95% CI 0·65–0·76]) and radical prostatectomy (4·0 [1·6–9·7]; p=0·0024; AUC 0·57 [0·52–0·61]) patients with prostate cancer, and its effect is magnified by intratumoral hypoxia (3·8 [1·2–12]; p=0·019; AUC 0·67 [0·61–0·73]). A novel 100-loci DNA signature accurately classified treatment outcome in the MSKCC low-risk to intermediate-risk cohort (multivariate analysis HR 6·1 [95% CI 2·0–19]; p=0·0015; AUC 0·74 [95% CI 0·65–0·83]). In the independent MSKCC and Cambridge cohorts, this signature identified low-risk to high-risk patients who were most likely to fail treatment within 18 months (combined cohorts multivariate analysis HR 2·9 [95% CI 1·4–6·0]; p=0·0039; AUC 0·68 [95% CI 0·63–0·73]), and was better at predicting biochemical relapse than 23 previously published RNA signatures. Interpretation This is the first study of cancer outcome to integrate DNA-based and microenvironment-based failure indices to predict patient outcome. Patients exhibiting these aggressive features after biopsy should be entered into treatment intensification trials. Funding Movember Foundation, Prostate Cancer Canada, Ontario Institute for Cancer Research, Canadian Institute for Health Research, NIHR Cambridge Biomedical Research Centre, The University of Cambridge, Cancer Research UK, Cambridge Cancer Charity, Prostate Cancer UK, Hutchison Whampoa Limited, Terry Fox Research Institute, Princess Margaret Cancer Centre Foundation, PMH-Radiation Medicine Program Academic Enrichment Fund, Motorcycle Ride for Dad (Durham), Canadian Cancer Society.
Author Collins, Colin C, Prof
Dal Pra, Alan, MD
Dunning, Mark J, PhD
Moon, Nathalie C, MMath
Fraser, Michael, PhD
Eeles, Rosalind, Prof
Davicioni, Elai, PhD
Milosevic, Michael, MD
Have, Cherry L, BSc
Squire, Jeremy A, Prof
Lalonde, Emilie, MSc
Chong, Lauren C, BCS
Bristow, Robert G, Prof
Thoms, John, MD
Neal, David E, Prof
Lam, Lucia L, BSc
Ramnarine, Varune R, BCS
Erho, Nicholas, MSc
van der Kwast, Theodorus, Prof
Berlin, Alejandro, MD
Ishkanian, Adrian S, MD
Mak, Denise Y F, PhD
Sykes, Jenna, MMath
Lamb, Alastair D, FRCS
Sendorek, Dorota H, BSc
Jurisica, Igor, Prof
Zafarana, Gaetano, PhD
Yao, Cindy Q, MSc
Xie, Honglei, MMath
P'ng, Christine, BSc
Malloff, Chad A, MSc
Grzadkowski, Michal R, BMath
Chu, Kenneth C, PhD
Warren, Anne Y, FRCPath
Cooper, Colin, PhD
Pintilie, Melania, MSc
Halim, Silvia, MSc
Meng, Xianyue, MSc
Ross-Adams, Helen, PhD
Harding, Nicholas J, PhD
Lam, Wan L, Prof
Boutros, Paul C, Prof
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25456371$$D View this record in MEDLINE/PubMed
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SSID ssj0017105
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Snippet Summary Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided...
Clinical prognostic groupings for localised prostate cancers are imprecise, with 30–50% of patients recurring after image-guided radiotherapy or radical...
Clinical prognostic groupings for localised prostate cancers are imprecise, with 30-50% of patients recurring after image-guided radiotherapy or radical...
Background Clinical prognostic groupings for localised prostate cancers are imprecise, with 30-50% of patients recurring after image-guided radiotherapy or...
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pubmed
elsevier
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StartPage 1521
SubjectTerms Antigens
Biomarkers, Tumor - genetics
Biopsy
Cancer therapies
Deoxyribonucleic acid
DNA
DNA, Neoplasm - genetics
Follow-Up Studies
Gene Expression Profiling
Genomes
Genomics
Hematology, Oncology and Palliative Medicine
Humans
Hypoxia
Male
Men
Metastasis
Mortality
Neoplasm Recurrence, Local - diagnosis
Neoplasm Recurrence, Local - genetics
Oligonucleotide Array Sequence Analysis
Patients
Prognosis
Prostate cancer
Prostatic Neoplasms - genetics
Radiation therapy
Retrospective Studies
Time Factors
Tumor Microenvironment - genetics
Title Tumour genomic and microenvironmental heterogeneity for integrated prediction of 5-year biochemical recurrence of prostate cancer: a retrospective cohort study
URI https://www.clinicalkey.es/playcontent/1-s2.0-S1470204514710216
https://dx.doi.org/10.1016/S1470-2045(14)71021-6
https://www.ncbi.nlm.nih.gov/pubmed/25456371
https://www.proquest.com/docview/1627109999
https://search.proquest.com/docview/1694978289
Volume 15
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