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Research Article

Temporal and Spatial Evolution of Somatic Chromosomal Alterations: A Case-Cohort Study of Barrett's Esophagus

Xiaohong Li, Patricia C. Galipeau, Thomas G. Paulson, Carissa A. Sanchez, Jessica Arnaudo, Karen Liu, Cassandra L. Sather, Rumen L. Kostadinov, Robert D. Odze, Mary K. Kuhner, Carlo C. Maley, Steven G. Self, Thomas L. Vaughan, Patricia L. Blount and Brian J. Reid
Xiaohong Li
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Patricia C. Galipeau
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Thomas G. Paulson
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Carissa A. Sanchez
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Jessica Arnaudo
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Karen Liu
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Cassandra L. Sather
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Rumen L. Kostadinov
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Robert D. Odze
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Mary K. Kuhner
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Carlo C. Maley
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Steven G. Self
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Thomas L. Vaughan
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Patricia L. Blount
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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Brian J. Reid
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
Divisions of 1Human Biology, 2Public Health Sciences, and 3Vaccine and Infectious Disease, Fred Hutchinson Cancer Research Center; Department of 4Genome Sciences, 5Epidemiology, and 6Medicine, University of Washington, Seattle, Washington; 7Genomics Resource, DNA Array Laboratory, Fred Hutchinson Cancer Research Center; 8Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland; 9Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; and 10Department of Surgery, Center for Evolution and Cancer, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California
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DOI: 10.1158/1940-6207.CAPR-13-0289 Published January 2014
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Abstract

All cancers are believed to arise by dynamic, stochastic somatic genomic evolution with genome instability, generation of diversity, and selection of genomic alterations that underlie multistage progression to cancer. Advanced esophageal adenocarcinomas have high levels of somatic copy number alterations. Barrett's esophagus is a risk factor for developing esophageal adenocarcinoma, and somatic chromosomal alterations (SCA) are known to occur in Barrett's esophagus. The vast majority (∼95%) of individuals with Barrett's esophagus do not progress to esophageal adenocarcinoma during their lifetimes, but a small subset develop esophageal adenocarcinoma, many of which arise rapidly even in carefully monitored patients without visible endoscopic abnormalities at the index endoscopy. Using a well-designed, longitudinal case-cohort study, we characterized SCA as assessed by single-nucleotide polymorphism arrays over space and time in 79 “progressors” with Barrett's esophagus as they approach the diagnosis of cancer and 169 “nonprogressors” with Barrett's esophagus who did not progress to esophageal adenocarcinoma over more than 20,425 person-months of follow-up. The genomes of nonprogressors typically had small localized deletions involving fragile sites and 9p loss/copy neutral LOH that generate little genetic diversity and remained relatively stable over prolonged follow-up. As progressors approach the diagnosis of cancer, their genomes developed chromosome instability with initial gains and losses, genomic diversity, and selection of SCAs followed by catastrophic genome doublings. Our results support a model of differential disease dynamics in which nonprogressor genomes largely remain stable over prolonged periods, whereas progressor genomes evolve significantly increased SCA and diversity within four years of esophageal adenocarcinoma diagnosis, suggesting a window of opportunity for early detection. Cancer Prev Res; 7(1); 114–27. ©2013 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Prevention Research Online (http://cancerprevres.aacrjournals.org/).

  • Received August 7, 2013.
  • Revision received October 1, 2013.
  • Accepted October 28, 2013.
  • ©2013 American Association for Cancer Research.
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January 2014
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Temporal and Spatial Evolution of Somatic Chromosomal Alterations: A Case-Cohort Study of Barrett's Esophagus
Xiaohong Li, Patricia C. Galipeau, Thomas G. Paulson, Carissa A. Sanchez, Jessica Arnaudo, Karen Liu, Cassandra L. Sather, Rumen L. Kostadinov, Robert D. Odze, Mary K. Kuhner, Carlo C. Maley, Steven G. Self, Thomas L. Vaughan, Patricia L. Blount and Brian J. Reid
Cancer Prev Res January 1 2014 (7) (1) 114-127; DOI: 10.1158/1940-6207.CAPR-13-0289

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Temporal and Spatial Evolution of Somatic Chromosomal Alterations: A Case-Cohort Study of Barrett's Esophagus
Xiaohong Li, Patricia C. Galipeau, Thomas G. Paulson, Carissa A. Sanchez, Jessica Arnaudo, Karen Liu, Cassandra L. Sather, Rumen L. Kostadinov, Robert D. Odze, Mary K. Kuhner, Carlo C. Maley, Steven G. Self, Thomas L. Vaughan, Patricia L. Blount and Brian J. Reid
Cancer Prev Res January 1 2014 (7) (1) 114-127; DOI: 10.1158/1940-6207.CAPR-13-0289
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