Differentially Expressed RNA from Public Microarray Data Identifies Serum Protein Biomarkers for Cross-Organ Transplant Rejection and Other Conditions
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{"title"=>"Differentially expressed RNA from public microarray data identifies serum protein biomarkers for cross-organ transplant rejection and other conditions", "type"=>"journal", "authors"=>[{"first_name"=>"Rong", "last_name"=>"Chen", "scopus_author_id"=>"55141261100"}, {"first_name"=>"Tara K.", "last_name"=>"Sigdel", "scopus_author_id"=>"6506057591"}, {"first_name"=>"Li", "last_name"=>"Li", "scopus_author_id"=>"56370080000"}, {"first_name"=>"Neeraja", "last_name"=>"Kambham", "scopus_author_id"=>"6603340119"}, {"first_name"=>"Joel T.", "last_name"=>"Dudley", "scopus_author_id"=>"18633685600"}, {"first_name"=>"Szu Chuan", "last_name"=>"Hsieh", "scopus_author_id"=>"7202057590"}, {"first_name"=>"R. Bryan", "last_name"=>"Klassen", "scopus_author_id"=>"57196648748"}, {"first_name"=>"Amery", "last_name"=>"Chen", "scopus_author_id"=>"57199685583"}, {"first_name"=>"Tuyen", "last_name"=>"Caohuu", "scopus_author_id"=>"37030708300"}, {"first_name"=>"Alexander A.", "last_name"=>"Morgan", "scopus_author_id"=>"35794613500"}, {"first_name"=>"Hannah A.", "last_name"=>"Valantine", "scopus_author_id"=>"35430802300"}, {"first_name"=>"Kiran K.", "last_name"=>"Khush", "scopus_author_id"=>"6505911383"}, {"first_name"=>"Minnie M.", "last_name"=>"Sarwal", "scopus_author_id"=>"12780413800"}, {"first_name"=>"Atul J.", "last_name"=>"Butte", "scopus_author_id"=>"7003333396"}], "year"=>2010, "source"=>"PLoS Computational Biology", "identifiers"=>{"sgr"=>"78049435079", "doi"=>"10.1371/journal.pcbi.1000940", "pui"=>"359882375", "pmid"=>"20885780", "scopus"=>"2-s2.0-78049435079", "issn"=>"1553734X", "isbn"=>"1553-7358 (Electronic)\\n1553-734X (Linking)"}, "id"=>"cc09facd-a972-3b17-be3c-cf26e2cd2979", "abstract"=>"Serum proteins are routinely used to diagnose diseases, but are hard to find due to low sensitivity in screening the serum proteome. Public repositories of microarray data, such as the Gene Expression Omnibus (GEO), contain RNA expression profiles for more than 16,000 biological conditions, covering more than 30% of United States mortality. We hypothesized that genes coding for serum- and urine-detectable proteins, and showing differential expression of RNA in disease-damaged tissues would make ideal diagnostic protein biomarkers for those diseases. We showed that predicted protein biomarkers are significantly enriched for known diagnostic protein biomarkers in 22 diseases, with enrichment significantly higher in diseases for which at least three datasets are available. We then used this strategy to search for new biomarkers indicating acute rejection (AR) across different types of transplanted solid organs. We integrated three biopsy-based microarray studies of AR from pediatric renal, adult renal and adult cardiac transplantation and identified 45 genes upregulated in all three. From this set, we chose 10 proteins for serum ELISA assays in 39 renal transplant patients, and discovered three that were significantly higher in AR. Interestingly, all three proteins were also significantly higher during AR in the 63 cardiac transplant recipients studied. Our best marker, serum PECAM1, identified renal AR with 89% sensitivity and 75% specificity, and also showed increased expression in AR by immunohistochemistry in renal, hepatic and cardiac transplant biopsies. Our results demonstrate that integrating gene expression microarray measurements from disease samples and even publicly-available data sets can be a powerful, fast, and cost-effective strategy for the discovery of new diagnostic serum protein biomarkers.", "link"=>"http://www.mendeley.com/research/differentially-expressed-rna-public-microarray-data-identifies-serum-protein-biomarkers-crossorgan-t", "reader_count"=>104, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>11, "Librarian"=>1, "Researcher"=>45, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Other"=>7, "Student > Master"=>6, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>5, "Professor > Associate Professor"=>11, "Librarian"=>1, "Researcher"=>45, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Other"=>7, "Student > Master"=>6, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>8, "Agricultural and Biological Sciences"=>41, "Business, Management and Accounting"=>1, "Chemical Engineering"=>1, "Chemistry"=>2, "Computer Science"=>7, "Engineering"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>10, "Medicine and Dentistry"=>25, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Psychology"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>25}, "Psychology"=>{"Psychology"=>2}, "Unspecified"=>{"Unspecified"=>8}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>1}, "Engineering"=>{"Engineering"=>2}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>41}, "Computer Science"=>{"Computer Science"=>7}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}}, "reader_count_by_country"=>{"Hong Kong"=>1, "United States"=>7, "United Kingdom"=>1, "Paraguay"=>1, "Australia"=>1, "Germany"=>3, "Spain"=>2}, "group_count"=>3}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/828995"], "description"=>"<p>(A) Acute rejection in a renal allograft biopsy with PECAM1 positive infiltrating lymphocytes and monocytes; endothelial cell staining occurred in glomeruli and peritubular capillaries. (B) In a stable graft renal allograft biopsy, PECAM1 staining occurred only in endothelial cells in glomeruli and peritubular capillaries. (C, E) Dense staining was observed in AR tissues after hepatic (C) and cardiac (E) transplants in infiltrating mononuclear cells and endothelial cells of capillaries and larger blood vessels. In hepatic (D) and cardiac (F) transplant biopsies from stable grafts, weak endothelial cell staining was observed (magnification ×400).</p>", "links"=>[], "tags"=>["pecam1", "staining", "acute", "rejection", "patients", "cardiac", "allograft"], "article_id"=>499345, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.g005", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_situ_PECAM1_staining_in_acute_rejection_and_stable_patients_in_renal_hepatic_and_cardiac_allograft_biopsies_/499345", "title"=>"<i>In situ</i> PECAM1 staining in acute rejection and stable patients in renal, hepatic, and cardiac allograft biopsies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-23 02:35:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/828606"], "description"=>"<p>We measured the protein concentration of ten genes by ELISA in independent serum samples of 19 AR patients and 20 patients with stable (STA) graft function after renal transplant. The protein concentrations of PECAM1 (A), CXCL9 (B), and CD44 (C) were higher in the AR serum samples, as shown in the notched boxplots. When the notches about two medians do not overlap, the medians are roughly significantly different at about a 95% confidence level <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000940#pcbi.1000940-McGill1\" target=\"_blank\">[54]</a> . The circles are outliers. P-values were calculated using the Mann-Whitney U test. One of the AR samples was inadvertently lost during the PECAM1 experiment and could not be recovered. (D) Areas under the Receiver Operating Characteristic (ROC) curves used to distinguish AR from STA were 0.811, 0.864, and 0.761 for PECAM1, CXCL9, and CD44, respectively.</p>", "links"=>[], "tags"=>["elisa", "biomarkers", "renal"], "article_id"=>498965, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Serum_ELISA_results_of_three_protein_biomarkers_in_renal_transplantation_/498965", "title"=>"Serum ELISA results of three protein biomarkers in renal transplantation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-23 02:29:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/828325"], "description"=>"<p>We calculated Fisher's exact test association p-values between predicted and known protein biomarkers for each of 41 diseases (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000940#pcbi-1000940-t001\" target=\"_blank\"><b>Table 1</b></a>). The values are plotted on the y-axis. Known protein biomarkers were more likely to be rediscovered (Mann-Whitney U p-value = 0.004) for the 11 diseases represented by ≥3 gene expression data sets (left notched box plot, median p-value = 5×10<sup>−4</sup>), versus those 30 diseases represented by <3 data sets (right, mean p-value = 0.12). A notch was added around the median p-value in each box to indicate the significance of difference. When the notches about two medians do not overlap, the medians are roughly significantly different at about a 95% confidence level <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000940#pcbi.1000940-McGill1\" target=\"_blank\">[54]</a> . The circles are outliers.</p>", "links"=>[], "tags"=>["biomarkers", "was"], "article_id"=>498679, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identifying_protein_biomarkers_was_more_likely_if_8805_3_gene_expression_data_were_available_/498679", "title"=>"Identifying protein biomarkers was more likely if ≥3 gene expression data were available.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-23 02:24:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/412513", "https://ndownloader.figshare.com/files/412551", "https://ndownloader.figshare.com/files/412602", "https://ndownloader.figshare.com/files/412646", "https://ndownloader.figshare.com/files/412676", "https://ndownloader.figshare.com/files/412707", "https://ndownloader.figshare.com/files/412736", "https://ndownloader.figshare.com/files/412753", "https://ndownloader.figshare.com/files/412770"], "description"=>"<div><p>Serum proteins are routinely used to diagnose diseases, but are hard to find due to low sensitivity in screening the serum proteome. Public repositories of microarray data, such as the Gene Expression Omnibus (GEO), contain RNA expression profiles for more than 16,000 biological conditions, covering more than 30% of United States mortality. We hypothesized that genes coding for serum- and urine-detectable proteins, and showing differential expression of RNA in disease-damaged tissues would make ideal diagnostic protein biomarkers for those diseases. We showed that predicted protein biomarkers are significantly enriched for known diagnostic protein biomarkers in 22 diseases, with enrichment significantly higher in diseases for which at least three datasets are available. We then used this strategy to search for new biomarkers indicating acute rejection (AR) across different types of transplanted solid organs. We integrated three biopsy-based microarray studies of AR from pediatric renal, adult renal and adult cardiac transplantation and identified 45 genes upregulated in all three. From this set, we chose 10 proteins for serum ELISA assays in 39 renal transplant patients, and discovered three that were significantly higher in AR. Interestingly, all three proteins were also significantly higher during AR in the 63 cardiac transplant recipients studied. Our best marker, serum PECAM1, identified renal AR with 89% sensitivity and 75% specificity, and also showed increased expression in AR by immunohistochemistry in renal, hepatic and cardiac transplant biopsies. Our results demonstrate that integrating gene expression microarray measurements from disease samples and even publicly-available data sets can be a powerful, fast, and cost-effective strategy for the discovery of new diagnostic serum protein biomarkers.</p></div>", "links"=>[], "tags"=>["differentially", "expressed", "rna", "microarray", "identifies", "serum", "biomarkers", "cross-organ", "transplant", "rejection", "conditions"], "article_id"=>141497, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1000940.s001", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s002", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s003", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s004", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s005", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s006", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s007", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s008", "https://dx.doi.org/10.1371/journal.pcbi.1000940.s009"], "stats"=>{"downloads"=>19, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Differentially_Expressed_RNA_from_Public_Microarray_Data_Identifies_Serum_Protein_Biomarkers_for_Cross_Organ_Transplant_Rejection_and_Other_Conditions/141497", "title"=>"Differentially Expressed RNA from Public Microarray Data Identifies Serum Protein Biomarkers for Cross-Organ Transplant Rejection and Other Conditions", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-09-23 00:24:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/829198"], "description"=>"<p>*Number of genes that were differentially expressed in any one of the disease tissues at the mRNA level (fpf≤0.05, RankProd R package) with detectable protein abundance in the biofluid proteome database (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000940#s4\" target=\"_blank\">Methods</a>).</p><p>*Number of known diagnostic protein biomarkers in clinical and preclinical studies from the GVK BIO Online Biomarker Database (GOBIOM).</p><p>**Number of correctly predicted diagnostic protein biomarkers.</p>$<p>P values were calculated to evaluate whether known protein biomarkers were significantly enriched in our predicted genes using Fisher's exact test.</p>", "links"=>[], "tags"=>["diagnostic", "biomarkers", "enriched", "sets", "differentially", "rna", "22", "41"], "article_id"=>499546, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.t001", "stats"=>{"downloads"=>8, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Known_diagnostic_protein_biomarkers_were_significantly_enriched_in_the_sets_of_differentially_expressed_RNA_for_22_out_of_41_diseases_/499546", "title"=>"Known diagnostic protein biomarkers were significantly enriched in the sets of differentially expressed RNA for 22 out of 41 diseases.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-23 02:39:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/828729"], "description"=>"<p>We measured the protein concentrations of PECAM1 (A), CXCL9 (B) and CD44 (C) by ELISA in the plasma of 32 AR patients and 31 STA patients after cardiac transplantation. All three proteins have statistically significantly higher concentration in the AR serum samples, compared to STA as shown in the notched box plots. P-values were calculated using the Mann-Whitney U test. (D) In ROC curves used to distinguish AR from STA, the areas under the curves were 0.716, 0.672, and 0.711 for PECAM1, CXCL, and CD44, respectively.</p>", "links"=>[], "tags"=>["elisa", "biomarkers", "cardiac"], "article_id"=>499083, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plasma_ELISA_of_three_protein_biomarkers_in_cardiac_transplantation_/499083", "title"=>"Plasma ELISA of three protein biomarkers in cardiac transplantation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-23 02:31:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/828488"], "description"=>"<p>We integrated three microarray studies examining gene expression after rejection in the biopsy samples from pediatric renal, adult renal, and adult heart transplants (the latter two were retrieved from GEO). We identified 45 genes that were upregulated in common in acute rejection compared to stable graft function. Among ten proteins we tested by ELISA, the concentrations of three were higher in serum samples from AR patients. The concentrations of the same three proteins were also higher in AR samples from cardiac transplantation. Immunohistochemistry showed that PECAM1 was increased in AR vs. stable biopsies in renal, hepatic and cardiac transplantation. All three biomarkers were from our identified AR pathway, and two of them showed detectable protein abundance in the biofluid proteome database we constructed before. CXCL9 was not listed in our biofluid proteome database, but is known to have detectable protein abundance <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000940#pcbi.1000940-Hauser1\" target=\"_blank\">[24]</a>.</p>", "links"=>[], "tags"=>["cross-organ", "ar", "biomarkers"], "article_id"=>498845, "categories"=>["Medicine", "Genetics"], "users"=>["Rong Chen", "Tara K. Sigdel", "Li Li", "Neeraja Kambham", "Joel T. Dudley", "Szu-chuan Hsieh", "R. Bryan Klassen", "Amery Chen", "Tuyen Caohuu", "Alexander A. Morgan", "Hannah A. Valantine", "Kiran K. Khush", "Minnie M. Sarwal", "Atul J. Butte"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000940.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_cross_organ_AR_protein_biomarkers_through_integration_of_gene_expression_data_/498845", "title"=>"Identification of cross-organ AR protein biomarkers through integration of gene expression data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-23 02:27:25"}

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  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"18", "cited-by"=>"1", "year"=>"2015", "month"=>"8"}
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  • {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
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  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
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  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"28", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
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  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"16", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"10", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"14", "full-text"=>"17", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
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  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"13", "full-text"=>"6", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
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  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"5", "cited-by"=>"1", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"33", "full-text"=>"10", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"9", "cited-by"=>"1", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"14", "full-text"=>"38", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"27", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"16", "full-text"=>"24", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"18", "cited-by"=>"2", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"17", "full-text"=>"42", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"18", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"19", "full-text"=>"19", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"9", "cited-by"=>"1", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"15", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"12", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"8", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"17", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"9", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}

Relative Metric

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