The evolution of non-small cell lung cancer metastases in TRACERx

Metastatic disease is responsible for the majority of cancer-related deaths 1 . We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of...

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Published inNature (London) Vol. 616; no. 7957; pp. 534 - 542
Main Authors Al Bakir, Maise, Huebner, Ariana, Martínez-Ruiz, Carlos, Grigoriadis, Kristiana, Watkins, Thomas B. K., Pich, Oriol, Moore, David A., Veeriah, Selvaraju, Ward, Sophia, Laycock, Joanne, Johnson, Diana, Rowan, Andrew, Razaq, Maryam, Akther, Mita, Naceur-Lombardelli, Cristina, Prymas, Paulina, Toncheva, Antonia, Hessey, Sonya, Dietzen, Michelle, Colliver, Emma, Frankell, Alexander M., Bunkum, Abigail, Lim, Emilia L., Karasaki, Takahiro, Abbosh, Christopher, Hiley, Crispin T., Hill, Mark S., Cook, Daniel E., Wilson, Gareth A., Salgado, Roberto, Nye, Emma, Stone, Richard Kevin, Fennell, Dean A., Price, Gillian, Kerr, Keith M., Naidu, Babu, Middleton, Gary, Summers, Yvonne, Lindsay, Colin R., Blackhall, Fiona H., Cave, Judith, Blyth, Kevin G., Nair, Arjun, Ahmed, Asia, Taylor, Magali N., Procter, Alexander James, Falzon, Mary, Lawrence, David, Navani, Neal, Thakrar, Ricky M., Janes, Sam M., Papadatos-Pastos, Dionysis, Forster, Martin D., Lee, Siow Ming, Ahmad, Tanya, Quezada, Sergio A., Peggs, Karl S., Van Loo, Peter, Dive, Caroline, Hackshaw, Allan, Birkbak, Nicolai J., Zaccaria, Simone, Jamal-Hanjani, Mariam, McGranahan, Nicholas, Swanton, Charles
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 20.04.2023
Nature Publishing Group
Subjects
45
45/22
45/23
631/114
631/181/2474
631/208/69
631/67/1612/1350
631/67/322
Cancer therapies
Carcinoma, Non-Small-Cell Lung - pathology
Clonal Evolution
Clone Cells - pathology
Cloning
Cohort Studies
Disease control
Disease Progression
Divergence
Evolution
Evolution, Molecular
Genomes
Humanities and Social Sciences
Humans
Lung cancer
Lung diseases
Lung Neoplasms - pathology
Lymph nodes
Lymphatic system
Mann-Whitney U test
Metastases
Metastasis
multidisciplinary
Mutation
Neoplasm Metastasis - diagnosis
Neoplasm Metastasis - pathology
Neoplasm Recurrence, Local
Non-small cell lung carcinoma
Patients
Positive selection
Quality control
Sampling
Science
Science (multidisciplinary)
Small cell lung carcinoma
Smoking
Tumors
Online AccessGet full text

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Abstract Metastatic disease is responsible for the majority of cancer-related deaths 1 . We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse. A longitudinal evolutionary analysis of 126 lung cancer patients with metastatic disease reveals the timing of metastatic divergence, modes of dissemination and the genomic events subject to selection during the metastatic transition.
AbstractList Metastatic disease is responsible for the majority of cancer-related deaths 1 . We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse. A longitudinal evolutionary analysis of 126 lung cancer patients with metastatic disease reveals the timing of metastatic divergence, modes of dissemination and the genomic events subject to selection during the metastatic transition.
Metastatic disease is responsible for the majority of cancer-related deaths 1 . We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.
Metastatic disease is responsible for the majority of cancer-related deaths . We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.
Metastatic disease is responsible for the majority of cancer-related deaths1. We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasisseeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site ofrecurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.
Metastatic disease is responsible for the majority of cancer-related deaths1. We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.Metastatic disease is responsible for the majority of cancer-related deaths1. We report the longitudinal evolutionary analysis of 126 non-small cell lung cancer (NSCLC) tumours from 421 prospectively recruited patients in TRACERx who developed metastatic disease, compared with a control cohort of 144 non-metastatic tumours. In 25% of cases, metastases diverged early, before the last clonal sweep in the primary tumour, and early divergence was enriched for patients who were smokers at the time of initial diagnosis. Simulations suggested that early metastatic divergence more frequently occurred at smaller tumour diameters (less than 8 mm). Single-region primary tumour sampling resulted in 83% of late divergence cases being misclassified as early, highlighting the importance of extensive primary tumour sampling. Polyclonal dissemination, which was associated with extrathoracic disease recurrence, was found in 32% of cases. Primary lymph node disease contributed to metastatic relapse in less than 20% of cases, representing a hallmark of metastatic potential rather than a route to subsequent recurrences/disease progression. Metastasis-seeding subclones exhibited subclonal expansions within primary tumours, probably reflecting positive selection. Our findings highlight the importance of selection in metastatic clone evolution within untreated primary tumours, the distinction between monoclonal versus polyclonal seeding in dictating site of recurrence, the limitations of current radiological screening approaches for early diverging tumours and the need to develop strategies to target metastasis-seeding subclones before relapse.
Author Wilson, Gareth A.
Ahmed, Asia
Prymas, Paulina
Janes, Sam M.
Veeriah, Selvaraju
Martínez-Ruiz, Carlos
Salgado, Roberto
Price, Gillian
Naidu, Babu
Hiley, Crispin T.
Zaccaria, Simone
Bunkum, Abigail
McGranahan, Nicholas
Cave, Judith
Hackshaw, Allan
Lindsay, Colin R.
Naceur-Lombardelli, Cristina
Ahmad, Tanya
Swanton, Charles
Summers, Yvonne
Nair, Arjun
Papadatos-Pastos, Dionysis
Middleton, Gary
Huebner, Ariana
Dietzen, Michelle
Nye, Emma
Hessey, Sonya
Jamal-Hanjani, Mariam
Colliver, Emma
Rowan, Andrew
Dive, Caroline
Fennell, Dean A.
Hill, Mark S.
Lim, Emilia L.
Peggs, Karl S.
Johnson, Diana
Cook, Daniel E.
Quezada, Sergio A.
Laycock, Joanne
Navani, Neal
Toncheva, Antonia
Kerr, Keith M.
Blyth, Kevin G.
Akther, Mita
Karasaki, Takahiro
Falzon, Mary
Frankell, Alexander M.
Abbosh, Christopher
Procter, Alexander James
Taylor, Magali N.
Blackhall, Fiona H.
Birkbak, Nicolai J.
Lee, Siow Ming
Lawrence, David
Grigoriadis, Kristiana
Razaq, Maryam
Al Bakir, Maise
Stone, Richard Kevin
Forster, Martin D.
Pich, Oriol
Moore, David A.
Watkins, Thomas B. K.
Ward, Soph
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  surname: McGranahan
  fullname: McGranahan, Nicholas
  email: nicholas.mcgranahan.10@ucl.ac.uk
  organization: Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, Cancer Genome Evolution Research Group, Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute
– sequence: 66
  givenname: Charles
  orcidid: 0000-0002-4299-3018
  surname: Swanton
  fullname: Swanton, Charles
  email: Charles.Swanton@crick.ac.uk
  organization: Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, Cancer Evolution and Genome Instability Laboratory, The Francis Crick Institute, Department of Oncology, University College London Hospitals
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37046095$$D View this record in MEDLINE/PubMed
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Schwarz, Roland F
Stavrou, Georgia
Castignani, Carla
Rosenthal, Rachel
Novasio, Juliette
Shackleford, Helen
Sokac, Mateo
Rane, Jayant K
Langman, Gerald
Rammohan, Kendadai
Weeden, Clare E
Cruickshank, Tracey
Sodha-Ramdeen, Azmina
Patel, Akshay J
Boyles, Rebecca
Leek, Angela
Montero, Angeles
Smith, Elaine
Magness, Alastair
Lowe, Helen L
Gomes, Fabio
Reading, James L
Pearce, David R
Stewart, Aengus
Lester, Jason F
Matharu, Gurdeep
Grönroos, Eva
Hodgkinson, Jack Davies
Rathinam, Sridhar
Diossy, Miklos
Kilgour, Elaine
Kadiri, Salma
Bishop, Paul
Campbell, Brittany B
Szallasi, Zoltan
Osman, Aya
Hoxha, Elena
Krebs, Matthew G
Rothwell, Dominic G
Totten, Nicola
Karamani, Angeliki
Cheyne, Heather
Dulloo, Sean
Levi, Dina
Kassiotis, George
Granato, Felice
Carter, Mathew
Aerts, Hugo J W L
Bajaj, Amrita
Kaufmann, Tom L
Zhai, Haoran
Larose Cadieux, Elizabeth
Khalil, Mohammed
Shah, Rajesh
Herrero, Javier
Gálvez-Cancino, Felip
Wilson, Claire
Lee, Claudia
Riley, Joan
Karagianni, Despoina
Joseph, Leena
Tugwood, Jonathan
Djearaman, Madava
Bailey, Chr
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Copyright The Author(s) 2023
2023. The Author(s).
Copyright Nature Publishing Group Apr 20, 2023
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– notice: 2023. The Author(s).
– notice: Copyright Nature Publishing Group Apr 20, 2023
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Snippet Metastatic disease is responsible for the majority of cancer-related deaths 1 . We report the longitudinal evolutionary analysis of 126 non-small cell lung...
Metastatic disease is responsible for the majority of cancer-related deaths . We report the longitudinal evolutionary analysis of 126 non-small cell lung...
Metastatic disease is responsible for the majority of cancer-related deaths1. We report the longitudinal evolutionary analysis of 126 non-small cell lung...
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SubjectTerms 45
45/22
45/23
631/114
631/181/2474
631/208/69
631/67/1612/1350
631/67/322
Cancer therapies
Carcinoma, Non-Small-Cell Lung - pathology
Clonal Evolution
Clone Cells - pathology
Cloning
Cohort Studies
Disease control
Disease Progression
Divergence
Evolution
Evolution, Molecular
Genomes
Humanities and Social Sciences
Humans
Lung cancer
Lung diseases
Lung Neoplasms - pathology
Lymph nodes
Lymphatic system
Mann-Whitney U test
Metastases
Metastasis
multidisciplinary
Mutation
Neoplasm Metastasis - diagnosis
Neoplasm Metastasis - pathology
Neoplasm Recurrence, Local
Non-small cell lung carcinoma
Patients
Positive selection
Quality control
Sampling
Science
Science (multidisciplinary)
Small cell lung carcinoma
Smoking
Tumors
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Title The evolution of non-small cell lung cancer metastases in TRACERx
URI https://link.springer.com/article/10.1038/s41586-023-05729-x
https://www.ncbi.nlm.nih.gov/pubmed/37046095
https://www.proquest.com/docview/2805592838
https://www.proquest.com/docview/2800627909
https://pubmed.ncbi.nlm.nih.gov/PMC10115651
Volume 616
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