Detection of Circulating Tumor DNA in Early- and Late-Stage Human Malignancies

Chetan Bettegowda; Mark Sausen; Rebecca J. Leary; Isaac Kinde; Yuxuan Wang; Nishant Agrawal; Bjarne R. Bartlett; Hao Wang; Brandon Luber; Rhoda M. Alani; Emmanuel S. Antonarakis; Nilofer S. Azad; Alberto Bardelli; Henry Brem; John L. Cameron; Clarence C. Lee; Leslie A. Fecher; Gary L. Gallia; Peter Gibbs; Dung Le; Robert L. Giuntoli; Michael Goggins; Michael D. Hogarty; Matthias Holdhoff; Seung-Mo Hong; Yuchen Jiao; Hartmut H. Juhl; Jenny J. Kim; Giulia Siravegna; Daniel A. Laheru; Calogero Lauricella; Michael Lim; Evan J. Lipson; Suely Kazue Nagahashi Marie; George J. Netto; Kelly S. Oliner; Alessandro Olivi; Louise Olsson; Gregory J. Riggins; Andrea Sartore-Bianchi; Kerstin Schmidt; le-Ming Shih; Sueli Mieko Oba-Shinjo; Salvatore Siena; Dan Theodorescu; Jeanne Tie; Timothy T. Harkins; Silvio Veronese; Tian-Li Wang; Jon D. Weingart; Christopher L. Wolfgang; Laura D. Wood; Dongmei Xing; Ralph H. Hruban; Jian Wu; Peter J. Allen; C. Max Schmidt; Michael A. Choti; Victor E. Velculescu; Kenneth W. Kinzler; Bert Vogelstein; Nickolas Papadopoulos; Luis A. Diaz

doi:10.1126/scitranslmed.3007094

Research ArticleCancer

Detection of Circulating Tumor DNA in Early- and Late-Stage Human Malignancies

Chetan Bettegowda¹,²,*,
Mark Sausen¹,*,†,
Rebecca J. Leary¹,*,‡,
Isaac Kinde¹,*,
Yuxuan Wang¹,
Nishant Agrawal¹,²,
Bjarne R. Bartlett¹,³,
Hao Wang¹,
Brandon Luber¹,
Rhoda M. Alani⁴,
Emmanuel S. Antonarakis¹,
Nilofer S. Azad¹,
Alberto Bardelli⁵,⁶,⁷,
Henry Brem²,
John L. Cameron²,
Clarence C. Lee⁸,
Leslie A. Fecher⁹,¹⁰,
Gary L. Gallia²,
Peter Gibbs¹¹,¹²,
Dung Le¹,³,
Robert L. Giuntoli²,
Michael Goggins²,
Michael D. Hogarty¹³,
Matthias Holdhoff¹,
Seung-Mo Hong²,¹⁴,
Yuchen Jiao¹,
Hartmut H. Juhl¹⁵,
Jenny J. Kim¹,
Giulia Siravegna¹⁶,
Daniel A. Laheru¹,
Calogero Lauricella¹⁶,
Michael Lim²,
Evan J. Lipson¹,
Suely Kazue Nagahashi Marie¹⁷,
George J. Netto²,
Kelly S. Oliner¹⁸,
Alessandro Olivi²,
Louise Olsson¹⁹,
Gregory J. Riggins²,
Andrea Sartore-Bianchi¹⁶,
Kerstin Schmidt¹,
le-Ming Shih²,
Sueli Mieko Oba-Shinjo¹⁷,
Salvatore Siena¹⁶,
Dan Theodorescu²⁰,
Jeanne Tie¹¹,
Timothy T. Harkins⁸,
Silvio Veronese¹⁶,
Tian-Li Wang²,
Jon D. Weingart²,
Christopher L. Wolfgang²,
Laura D. Wood²,
Dongmei Xing²,
Ralph H. Hruban²,
Jian Wu¹,²¹,§,
Peter J. Allen²²,
C. Max Schmidt²³,
Michael A. Choti²,¶,
Victor E. Velculescu¹,||,
Kenneth W. Kinzler¹,||,
Bert Vogelstein¹,||,
Nickolas Papadopoulos¹,|| and
Luis A. Diaz Jr¹,³,||

¹Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.
²Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
³Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.
⁴Department of Dermatology, Boston University, Boston, MA 02215, USA.
⁵Institute for Cancer Research and Treatment at Candiolo, University of Torino, Candiolo, Turin 10060, Italy.
⁶Department of Oncology, University of Torino, Candiolo, Turin 10060, Italy.
⁷FIRC Institute of Molecular Oncology (IFOM), Milan 20139, Italy.
⁸Advanced Applications and Collaborations, Life Technologies, Foster City, CA 94404, USA.
⁹Division of Oncology, University of Indiana, Indianapolis, IN 46202, USA.
¹⁰Indiana University Health, Indianapolis, IN 46202, USA.
¹¹Ludwig Institute for Cancer Research, Melbourne Branch, Royal Melbourne Hospital, Melbourne, Victoria 3084, Australia.
¹²Western Hospital, Melbourne, Victoria 3011, Australia.
¹³Division of Oncology, The Children’s Hospital of Philadelphia and the Department of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA.
¹⁴Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, Republic of Korea.
¹⁵Indivumed GmbH, Hamburg 20251, Germany.
¹⁶Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
¹⁷Department of Neurology and Pathology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil.
¹⁸Amgen Inc., Thousand Oaks, CA 91320, USA.
¹⁹Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm SE-171 76, Sweden.
²⁰University of Colorado Comprehensive Cancer Center, Aurora, CO 80045, USA.
²¹MyGenostics Inc., 801 West Baltimore Street, Baltimore, MD 21205, USA.
²²Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA.
²³Departments of Surgery, Biochemistry, and Molecular Biology, Indiana University, Indianapolis, IN 46202, USA.

↵||Corresponding authors. E-mail: ldiaz1{at}jhmi.edu (L.A.D.); npapado1{at}jhmi.edu (N.P.); vogelbe{at}jhmi.edu (B.V.); kinzlke{at}jhmi.edu (K.W.K.); velculescu{at}jhmi.edu (V.E.V.)

↵* These authors contributed equally to this work.
↵† Present address: Personal Genome Diagnostics, Baltimore, MD 21224, USA.
↵‡ Present address: Novartis Institutes for Biomedical Research, Cambridge, MA 02139, USA.
↵§ Present address: State Key Laboratory of Cancer Biology, Cell Engineering Research Center and Department of Cell Biology, The Fourth Military Medical University, Xi’an 710032, P. R. China.
↵¶ Present address: Department of Surgery University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

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Science Translational Medicine 19 Feb 2014:
Vol. 6, Issue 224, pp. 224ra24
DOI: 10.1126/scitranslmed.3007094

Chetan Bettegowda

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Mark Sausen

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Rebecca J. Leary

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Isaac Kinde

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Yuxuan Wang

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Nishant Agrawal

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Bjarne R. Bartlett

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.

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Hao Wang

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Brandon Luber

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Rhoda M. Alani

Department of Dermatology, Boston University, Boston, MA 02215, USA.

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Emmanuel S. Antonarakis

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Nilofer S. Azad

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Alberto Bardelli

Institute for Cancer Research and Treatment at Candiolo, University of Torino, Candiolo, Turin 10060, Italy.Department of Oncology, University of Torino, Candiolo, Turin 10060, Italy.FIRC Institute of Molecular Oncology (IFOM), Milan 20139, Italy.

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Henry Brem

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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John L. Cameron

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Clarence C. Lee

Advanced Applications and Collaborations, Life Technologies, Foster City, CA 94404, USA.

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Leslie A. Fecher

Division of Oncology, University of Indiana, Indianapolis, IN 46202, USA.Indiana University Health, Indianapolis, IN 46202, USA.

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Gary L. Gallia

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Peter Gibbs

Ludwig Institute for Cancer Research, Melbourne Branch, Royal Melbourne Hospital, Melbourne, Victoria 3084, Australia.Western Hospital, Melbourne, Victoria 3011, Australia.

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Dung Le

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.

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Robert L. Giuntoli

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Michael Goggins

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Michael D. Hogarty

Division of Oncology, The Children’s Hospital of Philadelphia and the Department of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA.

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Matthias Holdhoff

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Seung-Mo Hong

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, Republic of Korea.

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Yuchen Jiao

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Hartmut H. Juhl

Indivumed GmbH, Hamburg 20251, Germany.

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Jenny J. Kim

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Giulia Siravegna

Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.

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Daniel A. Laheru

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Calogero Lauricella

Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.

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Michael Lim

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Evan J. Lipson

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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Suely Kazue Nagahashi Marie

Department of Neurology and Pathology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil.

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George J. Netto

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Kelly S. Oliner

Amgen Inc., Thousand Oaks, CA 91320, USA.

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Alessandro Olivi

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Louise Olsson

Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm SE-171 76, Sweden.

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Gregory J. Riggins

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Andrea Sartore-Bianchi

Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.

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Kerstin Schmidt

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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le-Ming Shih

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Sueli Mieko Oba-Shinjo

Department of Neurology and Pathology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil.

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Salvatore Siena

Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.

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Dan Theodorescu

University of Colorado Comprehensive Cancer Center, Aurora, CO 80045, USA.

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Jeanne Tie

Ludwig Institute for Cancer Research, Melbourne Branch, Royal Melbourne Hospital, Melbourne, Victoria 3084, Australia.

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Timothy T. Harkins

Advanced Applications and Collaborations, Life Technologies, Foster City, CA 94404, USA.

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Silvio Veronese

Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.

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Tian-Li Wang

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Jon D. Weingart

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Christopher L. Wolfgang

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Laura D. Wood

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Dongmei Xing

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Ralph H. Hruban

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Jian Wu

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.MyGenostics Inc., 801 West Baltimore Street, Baltimore, MD 21205, USA.

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Peter J. Allen

Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA.

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C. Max Schmidt

Departments of Surgery, Biochemistry, and Molecular Biology, Indiana University, Indianapolis, IN 46202, USA.

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Michael A. Choti

Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.

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Victor E. Velculescu

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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For correspondence: ldiaz1@jhmi.edunpapado1@jhmi.eduvogelbe@jhmi.edukinzlke@jhmi.eduvelculescu@jhmi.edu

Kenneth W. Kinzler

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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For correspondence: ldiaz1@jhmi.edunpapado1@jhmi.eduvogelbe@jhmi.edukinzlke@jhmi.eduvelculescu@jhmi.edu

Bert Vogelstein

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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For correspondence: ldiaz1@jhmi.edunpapado1@jhmi.eduvogelbe@jhmi.edukinzlke@jhmi.eduvelculescu@jhmi.edu

Nickolas Papadopoulos

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.

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For correspondence: ldiaz1@jhmi.edunpapado1@jhmi.eduvogelbe@jhmi.edukinzlke@jhmi.eduvelculescu@jhmi.edu

Luis A. Diaz

Ludwig Center for Cancer Genetics and Therapeutics, Howard Hughes Medical Institute and the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.

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Circulating tumor DNA can be used in a variety of clinical and investigational settings across tumor types and stages for screening, diagnosis, and identifying mutations responsible for therapeutic response and drug resistance.

Detection of Circulating Tumor DNA in Early- and Late-Stage Human Malignancies

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