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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
Vol. 6, Issue 224, pp. 224ra24
DOI: 10.1126/scitranslmed.3007094
Chetan Bettegowda
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.
Mark Sausen
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.
Rebecca J. Leary
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.
Isaac Kinde
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.
Yuxuan Wang
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.
Nishant Agrawal
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.
Bjarne R. Bartlett
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.
3Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.
Hao Wang
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.
Brandon Luber
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.
Rhoda M. Alani
4Department of Dermatology, Boston University, Boston, MA 02215, USA.
Emmanuel S. Antonarakis
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.
Nilofer S. Azad
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.
Alberto Bardelli
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.
Henry Brem
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
John L. Cameron
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Clarence C. Lee
8Advanced Applications and Collaborations, Life Technologies, Foster City, CA 94404, USA.
Leslie A. Fecher
9Division of Oncology, University of Indiana, Indianapolis, IN 46202, USA.
10Indiana University Health, Indianapolis, IN 46202, USA.
Gary L. Gallia
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Peter Gibbs
11Ludwig Institute for Cancer Research, Melbourne Branch, Royal Melbourne Hospital, Melbourne, Victoria 3084, Australia.
12Western Hospital, Melbourne, Victoria 3011, Australia.
Dung Le
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.
3Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.
Robert L. Giuntoli
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Michael Goggins
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Michael D. Hogarty
13Division of Oncology, The Children’s Hospital of Philadelphia and the Department of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA.
Matthias Holdhoff
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.
Seung-Mo Hong
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
14Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, Republic of Korea.
Yuchen Jiao
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.
Hartmut H. Juhl
15Indivumed GmbH, Hamburg 20251, Germany.
Jenny J. Kim
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.
Giulia Siravegna
16Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
Daniel A. Laheru
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.
Calogero Lauricella
16Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
Michael Lim
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Evan J. Lipson
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.
Suely Kazue Nagahashi Marie
17Department of Neurology and Pathology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil.
George J. Netto
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Kelly S. Oliner
18Amgen Inc., Thousand Oaks, CA 91320, USA.
Alessandro Olivi
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Louise Olsson
19Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm SE-171 76, Sweden.
Gregory J. Riggins
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Andrea Sartore-Bianchi
16Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
Kerstin Schmidt
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.
le-Ming Shih
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Sueli Mieko Oba-Shinjo
17Department of Neurology and Pathology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil.
Salvatore Siena
16Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
Dan Theodorescu
20University of Colorado Comprehensive Cancer Center, Aurora, CO 80045, USA.
Jeanne Tie
11Ludwig Institute for Cancer Research, Melbourne Branch, Royal Melbourne Hospital, Melbourne, Victoria 3084, Australia.
Timothy T. Harkins
8Advanced Applications and Collaborations, Life Technologies, Foster City, CA 94404, USA.
Silvio Veronese
16Niguarda Cancer Center, Ospedale Niguarda Ca’ Granda, Milan 20162, Italy.
Tian-Li Wang
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Jon D. Weingart
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Christopher L. Wolfgang
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Laura D. Wood
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Dongmei Xing
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Ralph H. Hruban
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Jian Wu
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.
21MyGenostics Inc., 801 West Baltimore Street, Baltimore, MD 21205, USA.
Peter J. Allen
22Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA.
C. Max Schmidt
23Departments of Surgery, Biochemistry, and Molecular Biology, Indiana University, Indianapolis, IN 46202, USA.
Michael A. Choti
2Departments of Surgery, Medicine, Pathology, Obstetrics and Gynecology, Otolaryngology, and Neurosurgery at Johns Hopkins, Baltimore, MD 21231, USA.
Victor E. Velculescu
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.
Kenneth W. Kinzler
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.
Bert Vogelstein
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.
Nickolas Papadopoulos
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.
Luis A. Diaz Jr
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.
3Swim Across America Laboratory at Johns Hopkins, Baltimore, MD 21231, USA.
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