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Genomic Characterization of Brain Metastases Reveals Branched Evolution and Potential Therapeutic Targets

Priscilla K. Brastianos, Scott L. Carter, Sandro Santagata, Daniel P. Cahill, Amaro Taylor-Weiner, Robert T. Jones, Eliezer M. Van Allen, Michael S. Lawrence, Peleg M. Horowitz, Kristian Cibulskis, Keith L. Ligon, Josep Tabernero, Joan Seoane, Elena Martinez-Saez, William T. Curry, Ian F. Dunn, Sun Ha Paek, Sung-Hye Park, Aaron McKenna, Aaron Chevalier, Mara Rosenberg, Frederick G. Barker II, Corey M. Gill, Paul Van Hummelen, Aaron R. Thorner, Bruce E. Johnson, Mai P. Hoang, Toni K. Choueiri, Sabina Signoretti, Carrie Sougnez, Michael S. Rabin, Nancy U. Lin, Eric P. Winer, Anat Stemmer-Rachamimov, Matthew Meyerson, Levi Garraway, Stacey Gabriel, Eric S. Lander, Rameen Beroukhim, Tracy T. Batchelor, José Baselga, David N. Louis, Gad Getz and William C. Hahn
Priscilla K. Brastianos
1Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
2Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
3Cancer Center, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
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  • For correspondence: pbrastianos@partners.org william_hahn@dfci.harvard.edu carter.scott@jimmy.harvard.edu gadgetz@broadinstitute.org
Scott L. Carter
5Broad Institute, Boston, Massachusetts.
6Joint Center for Cancer Precision Medicine, Dana-Farber Cancer Institute, Boston, Massachusetts.
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  • For correspondence: pbrastianos@partners.org william_hahn@dfci.harvard.edu carter.scott@jimmy.harvard.edu gadgetz@broadinstitute.org
Sandro Santagata
7Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts.
8Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
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Daniel P. Cahill
9Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Amaro Taylor-Weiner
5Broad Institute, Boston, Massachusetts.
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Robert T. Jones
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
10Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Eliezer M. Van Allen
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
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Michael S. Lawrence
5Broad Institute, Boston, Massachusetts.
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Peleg M. Horowitz
11Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
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Kristian Cibulskis
5Broad Institute, Boston, Massachusetts.
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Keith L. Ligon
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
8Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
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Josep Tabernero
12Department of Medical Oncology, Vall d'Hebron University, Barcelona, Spain.
13Department of Pathology, Vall d'Hebron University, Barcelona, Spain.
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Joan Seoane
12Department of Medical Oncology, Vall d'Hebron University, Barcelona, Spain.
13Department of Pathology, Vall d'Hebron University, Barcelona, Spain.
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Elena Martinez-Saez
14Vall d'Hebron University Hospital and Institute of Oncology (VHIO), Barcelona, Spain.
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William T. Curry
9Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Ian F. Dunn
11Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
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Sun Ha Paek
15Department of Neurosurgery, Seoul National University College of Medicine, Seoul, South Korea.
16Department of Pathology, Seoul National University College of Medicine, Seoul, South Korea.
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Sung-Hye Park
15Department of Neurosurgery, Seoul National University College of Medicine, Seoul, South Korea.
16Department of Pathology, Seoul National University College of Medicine, Seoul, South Korea.
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Aaron McKenna
5Broad Institute, Boston, Massachusetts.
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Aaron Chevalier
5Broad Institute, Boston, Massachusetts.
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Mara Rosenberg
5Broad Institute, Boston, Massachusetts.
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Frederick G. Barker II
9Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Corey M. Gill
3Cancer Center, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Paul Van Hummelen
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
10Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Aaron R. Thorner
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
10Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Bruce E. Johnson
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Mai P. Hoang
17Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Toni K. Choueiri
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Sabina Signoretti
8Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
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Carrie Sougnez
5Broad Institute, Boston, Massachusetts.
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Michael S. Rabin
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Nancy U. Lin
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Eric P. Winer
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Anat Stemmer-Rachamimov
17Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Matthew Meyerson
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
8Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
10Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Levi Garraway
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
6Joint Center for Cancer Precision Medicine, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Stacey Gabriel
5Broad Institute, Boston, Massachusetts.
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Eric S. Lander
5Broad Institute, Boston, Massachusetts.
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Rameen Beroukhim
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
7Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Tracy T. Batchelor
2Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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José Baselga
18Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, New York.
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David N. Louis
17Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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Gad Getz
3Cancer Center, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
17Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
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  • For correspondence: pbrastianos@partners.org william_hahn@dfci.harvard.edu carter.scott@jimmy.harvard.edu gadgetz@broadinstitute.org
William C. Hahn
4Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
5Broad Institute, Boston, Massachusetts.
10Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts.
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  • For correspondence: pbrastianos@partners.org william_hahn@dfci.harvard.edu carter.scott@jimmy.harvard.edu gadgetz@broadinstitute.org
DOI: 10.1158/2159-8290.CD-15-0369 Published November 2015
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    Figure 1.

    Brain metastases harbor clinically actionable mutations not detected in primary-tumor samples. A–E, phylogenetic trees inferred for five example cases. Branch colors indicate the types of tissue samples descended from each branch (gray, shared by all samples; blue, primary-tumor sample; red, brain metastasis). Darker-colored lines correspond to subpopulations of cancer cells detected with CCF < 1; the maximally branching evolutionary relationships of these clusters are drawn on the ends of each sample branch, surrounded by shaded ellipses denoting the tissue sample. The thickness of each branch is proportional to the CCF of mutations on that branch. Potentially clinically informative (TARGET) alterations (black) and additional likely oncogenic alterations (gray) are annotated onto the phylogenetic branches on which they occurred. Timelines depict the sequence of diagnosis, treatment, and tissue sampling for each case, with chemotherapy treatment intervals denoted by gray rectangles, and treatment with specified targeted agents denoted by orange rectangles. Colored vertical lines denote collection of sequenced cancer tissues (blue, primary; red, brain metastasis). BEV, bevacizumab; BM, brain metastasis; BM1, brain metastasis from one anatomic location; BM2, brain metastasis from second anatomic location; Bx, biopsy; C, chemotherapy; CET, cetuximab; CR, complete response; Dx, diagnosis; EM, extracranial metastasis; I-131, radioactive iodine; LAP, lapatinib; LN, lymph node; PARPi, PARP inhibitor; PBM, progressive brain metastasis; PED, progressive extracranial disease; PI3Ki, PI3K inhibitor; SED, stable extracranial disease; Sx, surgery; SUN, sunitinib; TRA, trastuzumab; WBRT, whole brain radiotherapy; XRT, radiation. E, also shows immunohistochemical staining (IHC) for HER2 in samples of the primary tumor (left), and brain metastasis (right). In addition, genomic copy ratios on chromosome 17 are shown (bottom) for the primary-tumor sample (top) and brain metastasis (bottom). Large diamonds correspond to exons of ERBB2, colored according to amplification status (black, unamplified; red, amplified).

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    Figure 2.

    The landscape of potentially clinically actionable alterations in brain metastases and primary-tumor samples. A–D, alterations in genes (rows) that may predict sensitivity to the indicated class of targeted agent. Vertical columns correspond to cases, which are ordered by primary histology and presence/absence of alterations. Stacked bar graphs indicating the number of somatic point mutations detected in each phylogenetic branch of each case (columns) are shown at the top of each panel. HER2 status determined during clinical evaluation is denoted by: black, positive; gray, negative; white, not measured. COSMIC, Catalogue of Somatic Mutations in Cancer.

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    Figure 3.

    Anatomically and regionally distinct brain metastasis samples share actionable drivers. A–G, seven cases for which multiple regionally separated or anatomically distinct brain metastases were sequenced. The samples labeled R1, R2, etc., refer to different regions of the same pathology block. Phylogenetic trees and clinical histories are shown for each case as in Fig. 1. C and F, minor subclones shared by >1 tissue sample were detected (as described in the Methods). For these cases, the shared areas denote the tissue samples, and indicate which subclones are present in each sample. F and G, gadolinium-enhanced MRIs of the sampled brain metastases are shown.

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    Figure 4.

    Regional lymph nodes and distal extracranial metastases are not a reliable surrogate for actionable mutation in brain metastases. A–H, 8 cases for which at least one primary tumor sample, regional lymph node, and extracranial metastasis were sequenced. Phylogenetic trees and clinical histories are shown for each case as in Fig. 1. Tissue samples from extracranial metastases are depicted in green.

Additional Files

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  • Supplementary Data

    Files in this Data Supplement:

    • Supplementary Methods, Figures S1 - S20 - Supplementary Methods, Figures S1 - S20. Figure S1. Branched evolution leads to tissue-sampling bias in primary tumor samples. Figure S2. Results of ABSOLUTE on samples from patient 418. Figure S3. 2D Bayesian clustering analysis of point-mutation CCF distributions in case 418. Figure S4. Bayesian clustering of private point-mutation CCF distributions in all sequenced tissue samples from case 418. Figure S5. Genetic alterations supporting phylogeny construction in case 418. Figure S6. Phylogenetic tree for case 418 Figure S7. Evolutionary relationships between primary tumor-samples and brain metastasis samples Figure S8. Detection of homozygous deletion in CDKN2A in the brain metastasis of case 24. Figure S9. Amplification of FGFR1 and MYC detected in the brain metastasis of case 331. Figure S10. Additional alterations under investigation for association with various targeted therapies. Figure S11. Power for paired-detection of somatic mutations. Figure S12. Amplification of CCNE1 detected in the brain metastasis of case 314. Figure S13. Amplification of EGFR detected in the brain metastasis of case 314. Figure S14. Amplification of MYC detected in the brain metastasis of case 308. Figure S15. Amplification of MYC detected in the brain metastasis of case 138. Figure S16. Amplifications of CDK6 and MET detected in the brain metastasis of case 138. Figure S17. Amplifications of CCNE1 and AKT2 detected in the brain metastasis of case 138. Figure S18. Amplification of EGFR detected in a regional lymph node from case 296. Figure S19. Power for somatic mutation detection in 86 matched primary-tumor and brain-metastasis samples. Figure S20. Calling of amplifications in primary-tumor samples and paired brain metastases.
    • Supplementary File Legends - Supplementary File Legends
    • Supplementary Table S1 - Clinical characteristics of the 86 patients.
    • Supplementary Table S2 - Data describing results of deep targeted sequencing.
    • Supplementary Table S3 - Summary of clinically informative (TARGET) genes.
    • Supplementary File 1 - Supplementary File 1. Power for detection of somatic point mutations in coding exons of TARGET genes. The description for the plots in Supplementary File 1 can be found in the Legend of Supplementary Figure S1.
    • Supplementary File 2 - Supplementary File 2. Detailed plots of SCNA calls in TARGET genes. The description for the plots in Supplementary File 2 can be found in the Legend of Supplementary Figure S3.
    • Supplementary File 3 - Supplementary File 3. Detailed plots of the data used for phylogenetic inference in each case. The description for the plots in Supplementary File 3 can be found in the Legend of Supplementary Figure S13-S17.
  • Supplementary Data

    • Supplemental Material - Supplemental Material Supplementary Methods Supplementary figures Figure S1. Branched evolution leads to tissue-sampling bias in primary tumor samples Figure S2: Results of ABSOLUTE on samples from patient 418 Figure S3: 2D Bayesian clustering analysis of point-mutation CCF distributions in case 418 Figure S4: Bayesian clustering of private point-mutation CCF distributions in all sequenced tissue samples from case 418 Figure S5: Genetic alterations supporting phylogeny construction in case 418 Figure S6: Phylogenetic tree for case 418 Figure S7. Evolutionary relationships between primary tumor-samples and brain metastasis samples Figure S8. Detection of homozygous deletion in CDKN2A in the brain metastasis of case 24 Figure S9. Amplification of FGFR1 and MYC detected in the brain metastasis of case 331 Figure S10. Additional alterations under investigation for association with various targeted therapies Figure S11. Power for paired-detection of somatic mutations Figure S12. Amplification of CCNE1 detected in the brain metastasis of case 314 Figure S13. Amplification of EGFR detected in the brain metastasis of case 314 Figure S14. Amplification of MYC detected in the brain metastasis of case 308 Figure S15. Amplification of MYC detected in the brain metastasis of case 138 Figure S16. Amplifications of CDK6 and MET detected in the brain metastasis of case 138 Figure S17. Amplifications of CCNE1 and AKT2 detected in the brain metastasis of case 138 Figure S18. Amplification of EGFR detected in a regional lymph node from case 296 Figure S19. Power for somatic mutation detection in 86 matched primary-tumor and brain-metastasis samples. Figure S20. Calling of amplifications in primary-tumor samples and paired brain metastases.
    • Supplementary Table 1 - Clinical characteristics of the 86 patients
    • Supplementary Table 2 - Data describing results of deep targeted sequencing
    • Supplementary Table 3 - Summary of clinically informative (TARGET) genes
    • Legends for Supplementary Files 1-3 - Legends for Supplementary Files 1-3
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Cancer Discovery: 5 (11)
November 2015
Volume 5, Issue 11
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Genomic Characterization of Brain Metastases Reveals Branched Evolution and Potential Therapeutic Targets
Priscilla K. Brastianos, Scott L. Carter, Sandro Santagata, Daniel P. Cahill, Amaro Taylor-Weiner, Robert T. Jones, Eliezer M. Van Allen, Michael S. Lawrence, Peleg M. Horowitz, Kristian Cibulskis, Keith L. Ligon, Josep Tabernero, Joan Seoane, Elena Martinez-Saez, William T. Curry, Ian F. Dunn, Sun Ha Paek, Sung-Hye Park, Aaron McKenna, Aaron Chevalier, Mara Rosenberg, Frederick G. Barker II, Corey M. Gill, Paul Van Hummelen, Aaron R. Thorner, Bruce E. Johnson, Mai P. Hoang, Toni K. Choueiri, Sabina Signoretti, Carrie Sougnez, Michael S. Rabin, Nancy U. Lin, Eric P. Winer, Anat Stemmer-Rachamimov, Matthew Meyerson, Levi Garraway, Stacey Gabriel, Eric S. Lander, Rameen Beroukhim, Tracy T. Batchelor, José Baselga, David N. Louis, Gad Getz and William C. Hahn
Cancer Discov November 1 2015 (5) (11) 1164-1177; DOI: 10.1158/2159-8290.CD-15-0369

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Genomic Characterization of Brain Metastases Reveals Branched Evolution and Potential Therapeutic Targets
Priscilla K. Brastianos, Scott L. Carter, Sandro Santagata, Daniel P. Cahill, Amaro Taylor-Weiner, Robert T. Jones, Eliezer M. Van Allen, Michael S. Lawrence, Peleg M. Horowitz, Kristian Cibulskis, Keith L. Ligon, Josep Tabernero, Joan Seoane, Elena Martinez-Saez, William T. Curry, Ian F. Dunn, Sun Ha Paek, Sung-Hye Park, Aaron McKenna, Aaron Chevalier, Mara Rosenberg, Frederick G. Barker II, Corey M. Gill, Paul Van Hummelen, Aaron R. Thorner, Bruce E. Johnson, Mai P. Hoang, Toni K. Choueiri, Sabina Signoretti, Carrie Sougnez, Michael S. Rabin, Nancy U. Lin, Eric P. Winer, Anat Stemmer-Rachamimov, Matthew Meyerson, Levi Garraway, Stacey Gabriel, Eric S. Lander, Rameen Beroukhim, Tracy T. Batchelor, José Baselga, David N. Louis, Gad Getz and William C. Hahn
Cancer Discov November 1 2015 (5) (11) 1164-1177; DOI: 10.1158/2159-8290.CD-15-0369
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