Association of Angiopoietin-2 and Ki-67 Expression with Vascular Density and Sunitinib Response in Metastatic Renal Cell Carcinoma
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{"title"=>"Association of angiopoietin-2 and Ki-67 expression with vascular density and sunitinib response in metastatic renal cell carcinoma", "type"=>"journal", "authors"=>[{"first_name"=>"Juhana", "last_name"=>"Rautiola", "scopus_author_id"=>"37115982900"}, {"first_name"=>"Anita", "last_name"=>"Lampinen", "scopus_author_id"=>"56503622200"}, {"first_name"=>"Tuomas", "last_name"=>"Mirtti", "scopus_author_id"=>"6507566915"}, {"first_name"=>"Ari", "last_name"=>"Ristimäki", "scopus_author_id"=>"7006565915"}, {"first_name"=>"Heikki", "last_name"=>"Joensuu", "scopus_author_id"=>"7101710597"}, {"first_name"=>"Petri", "last_name"=>"Bono", "scopus_author_id"=>"7004432423"}, {"first_name"=>"Pipsa", "last_name"=>"Saharinen", "scopus_author_id"=>"6602910870"}], "year"=>2016, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "sgr"=>"84964762506", "doi"=>"10.1371/journal.pone.0153745", "scopus"=>"2-s2.0-84964762506", "pmid"=>"27100185", "pui"=>"610063683"}, "id"=>"645e7aa0-8a11-35ba-ae46-1dd913f09694", "abstract"=>"The Angiopoietin-2 (Ang2, Angpt2) growth factor is a context-dependent antagonist/agonist ligand of the endothelial Tie2 receptor tyrosine kinase and known to promote tumour angiogenesis and metastasis. Angiopoietin antagonists have been tested in clinical cancer trials in combination with VEGF-based anti-angiogenic therapy, including sunitinib, which is widely used as a first-line therapy for metastatic renal cell carcinoma (mRCC). However, little is known about Ang2 protein expression in human tumours and the correlation of tumour Ang2 expression with tumour vascularization, tumour cell proliferation and response to anti-angiogenic therapies. Here, we evaluated, using immunohistochemistry, the expression of Ang2, CD31 and the cell proliferation marker Ki-67 in the primary kidney cancer from 136 mRCC patients, who received first-line sunitinib after nephrectomy. Ang2 protein expression was restrained to RCC tumour vessels, and correlated with tumour vascularization and response to sunitinib. High pre-therapeutic Ang2 expression, and more strongly, combined high expression of both Ang2 and CD31, were associated with a high clinical benefit rate (CBR). Low cancer Ki-67 expression, but not Ang2 or CD31 expression, was associated with favourable progression-free (PFS) and overall survival (OS) as compared to patients with high Ki-67 expression (PFS 6.5 vs. 10.6 months, P = 0.009; OS, 15.7 vs. 28.5 months, P = 0.015). In summary, in this study to investigate endothelial Ang2 in mRCC patients treated with first-line sunitinib, high cancer Ang2 expression was associated with the CBR, but not PFS or OS, whereas low Ki-67 expression was significantly associated with long PFS and OS.", "link"=>"http://www.mendeley.com/research/association-angiopoietin2-ki67-expression-vascular-density-sunitinib-response-metastatic-renal-cell", "reader_count"=>10, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Librarian"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Student > Bachelor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Librarian"=>2, "Student > Ph. D. Student"=>1, "Student > Master"=>2, "Student > Bachelor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Medicine and Dentistry"=>5, "Psychology"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Finland"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/5001742"], "description"=>"<p>Immunohistochemical staining of mRCC primary tumour tissue using antibodies to Ang2 (<b>A</b>) and CD31 (<b>A, B</b>). (<b>A</b>) Representative images of mRCC tumours with negative (Ang2 = 0), weak (Ang2 = 1), moderate (Ang2 = 2) and high (Ang2 = 3) Ang2 expression scores, and their distribution in the Ang2 low (scores 0 and 1) and Ang2 high categories (scores 2 and 3) (top panel in A). Adjacent sections were stained for CD31 (bottom panel in A, scores not indicated). (<b>B</b>) Representative images of mRCC tumours with negative, weak, moderate (CD31 = 0, CD31 = 1, CD31 = 2) and high (CD31 = 3) CD31 expression scores, and their distribution in the CD31 low (scores 0–2) and CD31 high categories (score 3). (<b>C</b>) The percentage of patients with PR, SD and PD responses according to Ang2 expression scores 0–3, from negative (0) to high (3) expression. (<b>D-E</b>) High Ang2 (D) and high CD31 (E) protein expression in the mRCC tumour vasculature was associated with increased clinical benefit rate (CBR, PR/SD sunitinib responses) using Fisher’s exact test. (<b>F</b>) The percentage of patients with PR, SD and PD responses according to combined Ang2 and CD31 expression. (<b>G</b>) The combination of both high Ang2 and high CD31 protein expression was associated with increased CBR responses using Fisher’s exact test. PR, partial response; SD, stabilized disease; PD, progressive disease. Arrows indicate the magnified areas. Magnifications x100 and x400. Scale bar 80 μm.</p>", "links"=>[], "tags"=>["tumour cell proliferation", "cancer Ang 2 expression", "sunitinib", "Metastatic Renal Cell Carcinoma", "2 receptor tyrosine kinase", "CD 31 expression", "CBR", "136 mRCC patients", "RCC tumour vessels", "PFS 6.5 vs", "OS", "Ang 2 protein expression", "Ki", "Ang 2", "tumour vascularization", "tumour Ang 2 expression"], "article_id"=>3196129, "categories"=>["Medicine", "Chemical Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology", "Marine Biology", "Cancer"], "users"=>["Juhana Rautiola", "Anita Lampinen", "Tuomas Mirtti", "Ari Ristimäki", "Heikki Joensuu", "Petri Bono", "Pipsa Saharinen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153745.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Association_of_Ang2_and_CD31_expression_with_sunitinib_response_in_mRCC_/3196129", "title"=>"Association of Ang2 and CD31 expression with sunitinib response in mRCC.", "pos_in_sequence"=>3, "defined_type"=>1, "published_date"=>"2016-04-21 06:06:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001826"], "description"=>"<p>Patient Characteristics.</p>", "links"=>[], "tags"=>["tumour cell proliferation", "cancer Ang 2 expression", "sunitinib", "Metastatic Renal Cell Carcinoma", "2 receptor tyrosine kinase", "CD 31 expression", "CBR", "136 mRCC patients", "RCC tumour vessels", "PFS 6.5 vs", "OS", "Ang 2 protein expression", "Ki", "Ang 2", "tumour vascularization", "tumour Ang 2 expression"], "article_id"=>3196186, "categories"=>["Medicine", "Chemical Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology", "Marine Biology", "Cancer"], "users"=>["Juhana Rautiola", "Anita Lampinen", "Tuomas Mirtti", "Ari Ristimäki", "Heikki Joensuu", "Petri Bono", "Pipsa Saharinen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153745.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Patient_Characteristics_/3196186", "title"=>"Patient Characteristics.", "pos_in_sequence"=>5, "defined_type"=>3, "published_date"=>"2016-04-21 06:06:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001643", "https://ndownloader.figshare.com/files/5001658", "https://ndownloader.figshare.com/files/5001670", "https://ndownloader.figshare.com/files/5001676", "https://ndownloader.figshare.com/files/5001691"], "description"=>"<div><p>The Angiopoietin-2 (Ang2, Angpt2) growth factor is a context-dependent antagonist/agonist ligand of the endothelial Tie2 receptor tyrosine kinase and known to promote tumour angiogenesis and metastasis. Angiopoietin antagonists have been tested in clinical cancer trials in combination with VEGF-based anti-angiogenic therapy, including sunitinib, which is widely used as a first-line therapy for metastatic renal cell carcinoma (mRCC). However, little is known about Ang2 protein expression in human tumours and the correlation of tumour Ang2 expression with tumour vascularization, tumour cell proliferation and response to anti-angiogenic therapies. Here, we evaluated, using immunohistochemistry, the expression of Ang2, CD31 and the cell proliferation marker Ki-67 in the primary kidney cancer from 136 mRCC patients, who received first-line sunitinib after nephrectomy. Ang2 protein expression was restrained to RCC tumour vessels, and correlated with tumour vascularization and response to sunitinib. High pre-therapeutic Ang2 expression, and more strongly, combined high expression of both Ang2 and CD31, were associated with a high clinical benefit rate (CBR). Low cancer Ki-67 expression, but not Ang2 or CD31 expression, was associated with favourable progression-free (PFS) and overall survival (OS) as compared to patients with high Ki-67 expression (PFS 6.5 vs. 10.6 months, <i>P</i> = 0.009; OS, 15.7 vs. 28.5 months, <i>P</i> = 0.015). In summary, in this study to investigate endothelial Ang2 in mRCC patients treated with first-line sunitinib, high cancer Ang2 expression was associated with the CBR, but not PFS or OS, whereas low Ki-67 expression was significantly associated with long PFS and OS.</p></div>", "links"=>[], "tags"=>["tumour cell proliferation", "cancer Ang 2 expression", "sunitinib", "Metastatic Renal Cell Carcinoma", "2 receptor tyrosine kinase", "CD 31 expression", "CBR", "136 mRCC patients", "RCC tumour vessels", "PFS 6.5 vs", "OS", "Ang 2 protein expression", "Ki", "Ang 2", "tumour vascularization", "tumour Ang 2 expression"], "article_id"=>3196045, "categories"=>["Medicine", "Chemical Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology", "Marine Biology", "Cancer"], "users"=>["Juhana Rautiola", "Anita Lampinen", "Tuomas Mirtti", "Ari Ristimäki", "Heikki Joensuu", "Petri Bono", "Pipsa Saharinen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0153745.s001", "https://dx.doi.org/10.1371/journal.pone.0153745.s002", "https://dx.doi.org/10.1371/journal.pone.0153745.s003", "https://dx.doi.org/10.1371/journal.pone.0153745.s004", "https://dx.doi.org/10.1371/journal.pone.0153745.s005"], "stats"=>{"downloads"=>5, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Association_of_Angiopoietin_2_and_Ki_67_Expression_with_Vascular_Density_and_Sunitinib_Response_in_Metastatic_Renal_Cell_Carcinoma/3196045", "title"=>"Association of Angiopoietin-2 and Ki-67 Expression with Vascular Density and Sunitinib Response in Metastatic Renal Cell Carcinoma", "pos_in_sequence"=>1, "defined_type"=>4, "published_date"=>"2016-04-21 06:06:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001712"], "description"=>"<p><b>(A</b>) immunohistochemical staining of paraffin-embedded mRCC primary tumour tissue using a polyclonal antibody to Ang2. The CD31 expression was scored 3 in the sample. (<b>B</b>) An adjacent section was stained using the polyclonal antibody to Ang2, blocked with a 5-fold molar excess of recombinant human Ang2 (+rhAng2). Arrows indicate the magnified areas. Magnifications x200 and x400. Scale bar 40 μm.</p>", "links"=>[], "tags"=>["tumour cell proliferation", "cancer Ang 2 expression", "sunitinib", "Metastatic Renal Cell Carcinoma", "2 receptor tyrosine kinase", "CD 31 expression", "CBR", "136 mRCC patients", "RCC tumour vessels", "PFS 6.5 vs", "OS", "Ang 2 protein expression", "Ki", "Ang 2", "tumour vascularization", "tumour Ang 2 expression"], "article_id"=>3196102, "categories"=>["Medicine", "Chemical Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology", "Marine Biology", "Cancer"], "users"=>["Juhana Rautiola", "Anita Lampinen", "Tuomas Mirtti", "Ari Ristimäki", "Heikki Joensuu", "Petri Bono", "Pipsa Saharinen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153745.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Representative_immunohistochemical_staining_of_Ang2_in_mRCC_/3196102", "title"=>"Representative immunohistochemical staining of Ang2 in mRCC.", "pos_in_sequence"=>2, "defined_type"=>1, "published_date"=>"2016-04-21 06:06:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001778"], "description"=>"<p><b>(A)</b> Representative images of tumours with low Ki-67 expression (Ki-67+ nuclei % ≤10%), and high Ki-67 expression (Ki-67+ nuclei % >10%). (<b>B</b>) The distribution of patients according to Ki-67 expression, expressed as the % of Ki-67+nuclei. (<b>C-D</b>) Kaplan-Meier survival curves (Log rank) of progression-free (C) and cancer specific survival (D) in patients with low Ki-67 (blue) and high (green) Ki-67 expression scores. Arrows indicate the magnified areas. Magnifications x200 and x400. Scale bar 40 μm.</p>", "links"=>[], "tags"=>["tumour cell proliferation", "cancer Ang 2 expression", "sunitinib", "Metastatic Renal Cell Carcinoma", "2 receptor tyrosine kinase", "CD 31 expression", "CBR", "136 mRCC patients", "RCC tumour vessels", "PFS 6.5 vs", "OS", "Ang 2 protein expression", "Ki", "Ang 2", "tumour vascularization", "tumour Ang 2 expression"], "article_id"=>3196150, "categories"=>["Medicine", "Chemical Sciences not elsewhere classified", "Immunology", "Biological Sciences not elsewhere classified", "Developmental Biology", "Marine Biology", "Cancer"], "users"=>["Juhana Rautiola", "Anita Lampinen", "Tuomas Mirtti", "Ari Ristimäki", "Heikki Joensuu", "Petri Bono", "Pipsa Saharinen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153745.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Correlation_of_Ki_67_expression_with_progression_free_and_overall_survival_in_mRCC_in_response_to_first_line_sunitinib_/3196150", "title"=>"Correlation of Ki-67 expression with progression-free and overall survival in mRCC in response to first-line sunitinib.", "pos_in_sequence"=>4, "defined_type"=>1, "published_date"=>"2016-04-21 06:06:10"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"42", "full-text"=>"45", "pdf"=>"23", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"21", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"27", "full-text"=>"27", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"17", "full-text"=>"17", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"24", "full-text"=>"22", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"22", "full-text"=>"21", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"22", "full-text"=>"32", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"25", "full-text"=>"24", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"18", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"21", "full-text"=>"23", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"23", "full-text"=>"19", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"19", "full-text"=>"17", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"20", "full-text"=>"10", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"12", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"23", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"19", "full-text"=>"13", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"15", "full-text"=>"19", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"28", "full-text"=>"15", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"14", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"15", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"20", "full-text"=>"14", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"10", "pdf"=>"9", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"14", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"19", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"4", "full-text"=>"1", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"20", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"17", "full-text"=>"20", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}

Relative Metric

{"start_date"=>"2016-01-01T00:00:00Z", "end_date"=>"2016-12-31T00:00:00Z", "subject_areas"=>[]}
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