Tumor Mutation Burden Forecasts Outcome in Ovarian Cancer with BRCA1 or BRCA2 Mutations
Publication Date
November 12, 2013
Journal
PLOS ONE
Authors
Nicolai Juul Birkbak, Bose Kochupurakkal, Jose M. G. Izarzugaza, Aron C. Eklund, et al
Volume
8
Issue
11
Pages
e80023
DOI
https://dx.plos.org/10.1371/journal.pone.0080023
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0080023
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24265793
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3827141
Europe PMC
http://europepmc.org/abstract/MED/24265793
Web of Science
000327252100126
Scopus
84893049346
Mendeley
http://www.mendeley.com/research/tumor-mutation-burden-forecasts-outcome-ovarian-cancer-brca1-brca2-mutations
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Mendeley | Further Information

{"title"=>"Tumor mutation burden forecasts outcome in ovarian cancer with BRCA1 or BRCA2 mutations", "type"=>"journal", "authors"=>[{"first_name"=>"Nicolai Juul", "last_name"=>"Birkbak", "scopus_author_id"=>"37005365300"}, {"first_name"=>"Bose", "last_name"=>"Kochupurakkal", "scopus_author_id"=>"6507302907"}, {"first_name"=>"Jose M.G.", "last_name"=>"Izarzugaza", "scopus_author_id"=>"14219175600"}, {"first_name"=>"Aron C.", "last_name"=>"Eklund", "scopus_author_id"=>"8057455300"}, {"first_name"=>"Yang", "last_name"=>"Li", "scopus_author_id"=>"56018320300"}, {"first_name"=>"Joyce", "last_name"=>"Liu", "scopus_author_id"=>"35488204300"}, {"first_name"=>"Zoltan", "last_name"=>"Szallasi", "scopus_author_id"=>"7003492676"}, {"first_name"=>"Ursula A.", "last_name"=>"Matulonis", "scopus_author_id"=>"6701616188"}, {"first_name"=>"Andrea L.", "last_name"=>"Richardson", "scopus_author_id"=>"7402533820"}, {"first_name"=>"J. Dirk", "last_name"=>"Iglehart", "scopus_author_id"=>"7101868932"}, {"first_name"=>"Zhigang C.", "last_name"=>"Wang", "scopus_author_id"=>"7410046617"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84893049346", "doi"=>"10.1371/journal.pone.0080023", "pui"=>"372207792", "pmid"=>"24265793", "scopus"=>"2-s2.0-84893049346", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"700d76d4-a981-3050-a45b-98a4c56b6d81", "abstract"=>"BACKGROUND: Increased number of single nucleotide substitutions is seen in breast and ovarian cancer genomes carrying disease-associated mutations in BRCA1 or BRCA2. The significance of these genome-wide mutations is unknown. We hypothesize genome-wide mutation burden mirrors deficiencies in DNA repair and is associated with treatment outcome in ovarian cancer.\\n\\nMETHODS AND RESULTS: The total number of synonymous and non-synonymous exome mutations (Nmut), and the presence of germline or somatic mutation in BRCA1 or BRCA2 (mBRCA) were extracted from whole-exome sequences of high-grade serous ovarian cancers from The Cancer Genome Atlas (TCGA). Cox regression and Kaplan-Meier methods were used to correlate Nmut with chemotherapy response and outcome. Higher Nmut correlated with a better response to chemotherapy after surgery. In patients with mBRCA-associated cancer, low Nmut was associated with shorter progression-free survival (PFS) and overall survival (OS), independent of other prognostic factors in multivariate analysis. Patients with mBRCA-associated cancers and a high Nmut had remarkably favorable PFS and OS. The association with survival was similar in cancers with either BRCA1 or BRCA2 mutations. In cancers with wild-type BRCA, tumor Nmut was associated with treatment response in patients with no residual disease after surgery.\\n\\nCONCLUSIONS: Tumor Nmut was associated with treatment response and with both PFS and OS in patients with high-grade serous ovarian cancer carrying BRCA1 or BRCA2 mutations. In the TCGA cohort, low Nmut predicted resistance to chemotherapy, and for shorter PFS and OS, while high Nmut forecasts a remarkably favorable outcome in mBRCA-associated ovarian cancer. Our observations suggest that the total mutation burden coupled with BRCA1 or BRCA2 mutations in ovarian cancer is a genomic marker of prognosis and predictor of treatment response. This marker may reflect the degree of deficiency in BRCA-mediated pathways, or the extent of compensation for the deficiency by alternative mechanisms.", "link"=>"http://www.mendeley.com/research/tumor-mutation-burden-forecasts-outcome-ovarian-cancer-brca1-brca2-mutations", "reader_count"=>74, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>4, "Researcher"=>20, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>8, "Student > Bachelor"=>8, "Lecturer"=>4, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>4, "Researcher"=>20, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>8, "Student > Bachelor"=>8, "Lecturer"=>4, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>21, "Nursing and Health Professions"=>1, "Mathematics"=>1, "Agricultural and Biological Sciences"=>24, "Medicine and Dentistry"=>19, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>2, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>19}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>21}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1, "United Kingdom"=>1, "Nigeria"=>1, "Germany"=>1}, "group_count"=>5}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1277164"], "description"=>"<p>All patients received platinum and most received taxanes in combination. <b>A</b>) Tumors were separated into Nmut high and low groups defined by the median Nmut across the whole cohort and compared to the rate of chemotherapy resistance. The significance of the differences was determined by Fisher’s exact test. <b>B</b>) The number of mutations (Nmut) for each tumor was compared in chemotherapy resistant and sensitive patients and is shown by dot plots. Median and 25-75 percentiles are indicated by horizontal lines. P-value is derived from the Wilcoxon rank-sum test. <b>C</b>) Kaplan-Meier analysis compared the progression-free survival (PFS) and <b>D</b>) overall survival (OS) between patients with high and low tumor Nmut. Patients that were progression-free or still alive at the time of last follow-up were censored (+). Numbers of patients at risk at each interval are given below the graphs. P-values are obtained by Log-rank test.</p>", "links"=>[], "tags"=>["exome", "mutations", "high-grade", "serous", "ovarian"], "article_id"=>847784, "categories"=>["Biological Sciences"], "users"=>["Nicolai Juul Birkbak", "Bose Kochupurakkal", "José M. G. Izarzugaza", "Aron C. Eklund", "Yang Li", "Joyce Liu", "Zoltan Szallasi", "Ursula A. Matulonis", "Andrea L. Richardson", "J. Dirk Iglehart", "Zhigang C. Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080023.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Total_number_of_exome_mutations_Nmut_and_clinical_outcome_in_high_grade_serous_ovarian_cancer_/847784", "title"=>"Total number of exome mutations (Nmut) and clinical outcome in high-grade serous ovarian cancer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-12 03:21:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1277172", "https://ndownloader.figshare.com/files/1277173", "https://ndownloader.figshare.com/files/1277174", "https://ndownloader.figshare.com/files/1277175", "https://ndownloader.figshare.com/files/1277176", "https://ndownloader.figshare.com/files/1277177", "https://ndownloader.figshare.com/files/1277178", "https://ndownloader.figshare.com/files/1277179", "https://ndownloader.figshare.com/files/1277180"], "description"=>"<div><p>Background</p><p>Increased number of single nucleotide substitutions is seen in breast and ovarian cancer genomes carrying disease-associated mutations in <i>BRCA1</i> or <i>BRCA2</i>. The significance of these genome-wide mutations is unknown. We hypothesize genome-wide mutation burden mirrors deficiencies in DNA repair and is associated with treatment outcome in ovarian cancer.</p> <p>Methods and Results</p><p>The total number of synonymous and non-synonymous exome mutations (Nmut), and the presence of germline or somatic mutation in <i>BRCA1</i> or <i>BRCA2</i> (mBRCA) were extracted from whole-exome sequences of high-grade serous ovarian cancers from The Cancer Genome Atlas (TCGA). Cox regression and Kaplan-Meier methods were used to correlate Nmut with chemotherapy response and outcome. Higher Nmut correlated with a better response to chemotherapy after surgery. In patients with mBRCA-associated cancer, low Nmut was associated with shorter progression-free survival (PFS) and overall survival (OS), independent of other prognostic factors in multivariate analysis. Patients with mBRCA-associated cancers and a high Nmut had remarkably favorable PFS and OS. The association with survival was similar in cancers with either <i>BRCA1</i> or <i>BRCA2</i> mutations. In cancers with wild-type BRCA, tumor Nmut was associated with treatment response in patients with no residual disease after surgery.</p> <p>Conclusions</p><p>Tumor Nmut was associated with treatment response and with both PFS and OS in patients with high-grade serous ovarian cancer carrying <i>BRCA1</i> or <i>BRCA2</i> mutations. In the TCGA cohort, low Nmut predicted resistance to chemotherapy, and for shorter PFS and OS, while high Nmut forecasts a remarkably favorable outcome in mBRCA-associated ovarian cancer. Our observations suggest that the total mutation burden coupled with <i>BRCA1</i> or <i>BRCA2</i> mutations in ovarian cancer is a genomic marker of prognosis and predictor of treatment response. This marker may reflect the degree of deficiency in BRCA-mediated pathways, or the extent of compensation for the deficiency by alternative mechanisms.</p> </div>", "links"=>[], "tags"=>["mutation", "forecasts", "ovarian", "cancer", "BRCA1", "brca2"], "article_id"=>847789, "categories"=>["Biological Sciences"], "users"=>["Nicolai Juul Birkbak", "Bose Kochupurakkal", "José M. G. Izarzugaza", "Aron C. Eklund", "Yang Li", "Joyce Liu", "Zoltan Szallasi", "Ursula A. Matulonis", "Andrea L. Richardson", "J. Dirk Iglehart", "Zhigang C. Wang"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0080023.s001", "https://dx.doi.org/10.1371/journal.pone.0080023.s002", "https://dx.doi.org/10.1371/journal.pone.0080023.s003", "https://dx.doi.org/10.1371/journal.pone.0080023.s004", "https://dx.doi.org/10.1371/journal.pone.0080023.s005", "https://dx.doi.org/10.1371/journal.pone.0080023.s006", "https://dx.doi.org/10.1371/journal.pone.0080023.s007", "https://dx.doi.org/10.1371/journal.pone.0080023.s008", "https://dx.doi.org/10.1371/journal.pone.0080023.s009"], "stats"=>{"downloads"=>15, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tumor_Mutation_Burden_Forecasts_Outcome_in_Ovarian_Cancer_with_BRCA1_or_BRCA2_Mutations_/847789", "title"=>"Tumor Mutation Burden Forecasts Outcome in Ovarian Cancer with BRCA1 or BRCA2 Mutations", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-11-12 03:21:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1277167"], "description"=>"<p>Nmut high and low were defined by values above or below the median Nmut from all wtBRCA tumors in the cohort. <b>A</b>) Kaplan-Meier analysis compared PFS, and <b>B</b>) OS between tumor Nmut high and low in patients with wtBRCA tumors and no residual disease after debulking surgery. Numbers of patients at risk at each interval are given below the graphs. P-values are obtained from Log-rank test.</p>", "links"=>[], "tags"=>["patients", "wtbrca", "tumors", "residual"], "article_id"=>847787, "categories"=>["Biological Sciences"], "users"=>["Nicolai Juul Birkbak", "Bose Kochupurakkal", "José M. G. Izarzugaza", "Aron C. Eklund", "Yang Li", "Joyce Liu", "Zoltan Szallasi", "Ursula A. Matulonis", "Andrea L. Richardson", "J. Dirk Iglehart", "Zhigang C. Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080023.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nmut_and_treatment_outcome_in_patients_with_wtBRCA_tumors_and_no_residual_disease_after_initial_surgery_/847787", "title"=>"Nmut and treatment outcome in patients with wtBRCA tumors and no residual disease after initial surgery.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-12 03:21:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1277165"], "description"=>"<p><b>A</b>) Nmut in tumors with mBRCA. Chemotherapy resistant and sensitive ovarian cancers are shown by dot plots. P-value is derived from the Wilcoxon rank-sum test. <b>B</b>) Nmut in tumors with wtBRCA. Chemotherapy resistant and sensitive tumors are shown with dot plots of each tumor as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080023#pone-0080023-g001\" target=\"_blank\">Figure 1</a>. Median and 25-75 percentiles are indicated by horizontal lines. P-value is derived from Wilcoxon rank-sum test. <b>C</b>) Kaplan-Meier analysis compared PFS and <b>D</b>) OS between patients with high and low Nmut in their mBRCA-associated tumors. <b>E</b>) Kaplan-Meier analysis compared PFS and <b>F</b>) OS in patients with high and low Nmut in their wtBRCA tumors. The median for Nmut was computed from the whole cohort of 316 tumors. In Kaplan-Meier analyses, patients that were progression-free or still alive at the time of last follow-up were censored (+). Numbers of patients at risk at each interval are given below the graphs. P-values are obtained from Log-rank test.</p>", "links"=>[], "tags"=>["exome", "mutations", "high-grade", "serous", "ovarian", "cancer", "germline", "somatic", "wild-type"], "article_id"=>847785, "categories"=>["Biological Sciences"], "users"=>["Nicolai Juul Birkbak", "Bose Kochupurakkal", "José M. G. Izarzugaza", "Aron C. Eklund", "Yang Li", "Joyce Liu", "Zoltan Szallasi", "Ursula A. Matulonis", "Andrea L. Richardson", "J. Dirk Iglehart", "Zhigang C. Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080023.g002", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Total_number_of_exome_mutations_Nmut_and_clinical_outcome_in_high_grade_serous_ovarian_cancer_with_germline_or_somatic_mutations_in_BRCA1_or_BRCA2_mBRCA_or_with_wild_type_BRCA1_and_BRCA2_wtBRCA_/847785", "title"=>"Total number of exome mutations (Nmut) and clinical outcome in high-grade serous ovarian cancer with germline or somatic mutations in <i>BRCA1</i> or <i>BRCA2</i> (mBRCA) or with wild-type <i>BRCA1</i> and <i>BRCA2</i> (wtBRCA).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-12 03:21:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1277166"], "description"=>"<p><b>A</b>) Kaplan-Meier analysis compared PFS and <b>B</b>) OS between Nmut high and low ovarian cancers, all of which carried either a <i>BRCA1</i> or <i>BRCA2</i> germline mutation with LOH at the corresponding BRCA locus. <b>C</b> - <b>F</b>) Analysis in individual BRCA1 and BRCA2 mutation carrier groups. <b>C</b>) Kaplan-Meier analysis in patients with <i>BRCA1</i>-associated tumors comparing PFS, and <b>D</b>) OS. <b>E</b>) Kaplan-Meier analysis in patients with <i>BRCA2</i>-associated tumors comparing PFS, and <b>F</b>) OS. Nmut high and low are defined as a value above or below median Nmut of all mBRCA-associated tumors. Numbers of patients at risk at each interval are given below the graphs. <i>P</i>-values are calculated by log-rank test. </p>", "links"=>[], "tags"=>["nmut", "ovarian", "cancer", "patients", "carrying", "brca", "germline", "mutations", "loh", "loci"], "article_id"=>847786, "categories"=>["Biological Sciences"], "users"=>["Nicolai Juul Birkbak", "Bose Kochupurakkal", "José M. G. Izarzugaza", "Aron C. Eklund", "Yang Li", "Joyce Liu", "Zoltan Szallasi", "Ursula A. Matulonis", "Andrea L. Richardson", "J. Dirk Iglehart", "Zhigang C. Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0080023.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tumor_Nmut_and_clinical_treatment_outcome_in_ovarian_cancer_patients_carrying_BRCA_germline_mutations_with_LOH_at_the_BRCA_loci_in_tumors_/847786", "title"=>"Tumor Nmut and clinical treatment outcome in ovarian cancer patients carrying BRCA germline mutations with LOH at the BRCA loci in tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-12 03:21:43"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Medicine and health sciences/Oncology", "average_usage"=>[249, 468, 599, 718, 820, 920, 1008, 1093, 1181, 1281, 1357, 1444, 1517]}, {"subject_area"=>"/Medicine and health sciences/Pharmaceutics", "average_usage"=>[254, 457, 591, 700, 808, 906, 1001, 1093, 1185, 1276, 1373, 1457, 1535]}, {"subject_area"=>"/Medicine and health sciences/Surgical and invasive medical procedures", "average_usage"=>[223, 396, 511, 599, 690, 775, 859, 936, 1012, 1090, 1168, 1237, 1299]}]}
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