Transforming Growth Factor Beta 2 and Heme Oxygenase 1 Genes Are Risk Factors for the Cerebral Malaria Syndrome in Angolan Children
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{"title"=>"Transforming growth factor beta 2 and heme oxygenase 1 genes are risk factors for the cerebral malaria syndrome in Angolan children", "type"=>"journal", "authors"=>[{"first_name"=>"Maria Rosário", "last_name"=>"Sambo", "scopus_author_id"=>"36627575200"}, {"first_name"=>"Maria Jesus", "last_name"=>"Trovoada", "scopus_author_id"=>"6507773665"}, {"first_name"=>"Carla", "last_name"=>"Benchimol", "scopus_author_id"=>"14046802800"}, {"first_name"=>"Vatúsia", "last_name"=>"Quinhentos", "scopus_author_id"=>"14047401100"}, {"first_name"=>"Lígia", "last_name"=>"Gonçalves", "scopus_author_id"=>"14719557400"}, {"first_name"=>"Rute", "last_name"=>"Velosa", "scopus_author_id"=>"57199610749"}, {"first_name"=>"Maria Isabel", "last_name"=>"Marques", "scopus_author_id"=>"57197594189"}, {"first_name"=>"Nuno", "last_name"=>"Sepúlveda", "scopus_author_id"=>"25625488800"}, {"first_name"=>"Taane G.", "last_name"=>"Clark", "scopus_author_id"=>"7403216793"}, {"first_name"=>"Stefan", "last_name"=>"Mustafa", "scopus_author_id"=>"7101717457"}, {"first_name"=>"Oswald", "last_name"=>"Wagner", "scopus_author_id"=>"7102433639"}, {"first_name"=>"António", "last_name"=>"Coutinho", "scopus_author_id"=>"7102909682"}, {"first_name"=>"Carlos", "last_name"=>"Penha-Gonçalves", "scopus_author_id"=>"6602527631"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"359293481", "sgr"=>"77955253432", "pmid"=>"20585394", "scopus"=>"2-s2.0-77955253432", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0011141", "issn"=>"19326203"}, "id"=>"7c24c608-7828-344a-8856-ec159647a7e9", "abstract"=>"BACKGROUND Cerebral malaria (CM) represents a severe outcome of the Plasmodium falciparum infection. Recent genetic studies have correlated human genes with severe malaria susceptibility, but there is little data on genetic variants that increase the risk of developing specific malaria clinical complications. Nevertheless, susceptibility to experimental CM in the mouse has been linked to host genes including Transforming Growth Factor Beta 2 (TGFB2) and Heme oxygenase-1 (HMOX1). Here, we tested whether those genes were governing the risk of progressing to CM in patients with severe malaria syndromes. METHODOLOGY/PRINCIPAL FINDINGS We report that the clinical outcome of P. falciparum infection in a cohort of Angolan children (n = 430) correlated with nine TGFB2 SNPs that modify the risk of progression to CM as compared to other severe forms of malaria. This genetic effect was explained by two haplotypes harboring the CM-associated SNPs (Pcorrec. = 0.035 and 0.036). In addition, one HMOX1 haplotype composed of five CM-associated SNPs increased the risk of developing the CM syndrome (Pcorrec. = 0.002) and was under-transmitted to children with uncomplicated malaria (P = 0.036). Notably, the HMOX1-associated haplotype conferred increased HMOX1 mRNA expression in peripheral blood cells of CM patients (P = 0.012). CONCLUSIONS/SIGNIFICANCE These results represent the first report on CM genetic risk factors in Angolan children and suggest the novel hypothesis that genetic variants of the TGFB2 and HMOX1 genes may contribute to confer a specific risk of developing the CM syndrome in patients with severe P. falciparum malaria. This work may provide motivation for future studies aiming to replicate our findings in larger populations and to confirm a role for these genes in determining the clinical course of malaria.", "link"=>"http://www.mendeley.com/research/transforming-growth-factor-beta-2-heme-oxygenase-1-genes-risk-factors-cerebral-malaria-syndrome-ango-4", "reader_count"=>30, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>14, "Medicine and Dentistry"=>8, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Psychology"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"Saudi Arabia"=>1, "United States"=>1, "Brazil"=>1, "Italy"=>1, "United Kingdom"=>1, "France"=>1, "Portugal"=>1}, "group_count"=>1}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/420633", "https://ndownloader.figshare.com/files/420670", "https://ndownloader.figshare.com/files/420702", "https://ndownloader.figshare.com/files/420726"], "description"=>"<div><h3>Background</h3><p>Cerebral malaria (CM) represents a severe outcome of the <em>Plasmodium falciparum</em> infection. Recent genetic studies have correlated human genes with severe malaria susceptibility, but there is little data on genetic variants that increase the risk of developing specific malaria clinical complications. Nevertheless, susceptibility to experimental CM in the mouse has been linked to host genes including <em>Transforming Growth Factor Beta 2 (TGFB2)</em> and <em>Heme oxygenase-1 (HMOX1)</em>. Here, we tested whether those genes were governing the risk of progressing to CM in patients with severe malaria syndromes.</p><h3>Methodology/Principal Findings</h3><p>We report that the clinical outcome of <em>P. falciparum</em> infection in a cohort of Angolan children (n = 430) correlated with nine <em>TGFB2</em> SNPs that modify the risk of progression to CM as compared to other severe forms of malaria. This genetic effect was explained by two haplotypes harboring the CM-associated SNPs (Pcorrec. = 0.035 and 0.036). In addition, one <em>HMOX1</em> haplotype composed of five CM-associated SNPs increased the risk of developing the CM syndrome (Pcorrec. = 0.002) and was under-transmitted to children with uncomplicated malaria (P = 0.036). Notably, the <em>HMOX1</em>-associated haplotype conferred increased <em>HMOX1</em> mRNA expression in peripheral blood cells of CM patients (P = 0.012).</p><h3>Conclusions/Significance</h3><p>These results represent the first report on CM genetic risk factors in Angolan children and suggest the novel hypothesis that genetic variants of the <em>TGFB2</em> and <em>HMOX1</em> genes may contribute to confer a specific risk of developing the CM syndrome in patients with severe <em>P. falciparum</em> malaria. This work may provide motivation for future studies aiming to replicate our findings in larger populations and to confirm a role for these genes in determining the clinical course of malaria.</p></div>", "links"=>[], "tags"=>["transforming", "beta", "heme", "oxygenase", "genes", "are", "factors", "cerebral", "malaria", "angolan", "children"], "article_id"=>143040, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011141.s001", "https://dx.doi.org/10.1371/journal.pone.0011141.s002", "https://dx.doi.org/10.1371/journal.pone.0011141.s003", "https://dx.doi.org/10.1371/journal.pone.0011141.s004"], "stats"=>{"downloads"=>6, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Transforming_Growth_Factor_Beta_2_and_Heme_Oxygenase_1_Genes_Are_Risk_Factors_for_the_Cerebral_Malaria_Syndrome_in_Angolan_Children/143040", "title"=>"Transforming Growth Factor Beta 2 and Heme Oxygenase 1 Genes Are Risk Factors for the Cerebral Malaria Syndrome in Angolan Children", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-06-16 00:50:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/844662"], "description"=>"<p>Beta, genetic effect under logistic regression model; Stat, test statistic; P, empirical p-value.</p>", "links"=>[], "tags"=>["quantitative", "cerebral", "malaria"], "article_id"=>515099, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.t005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Haplotypic_quantitative_trait_analysis_of_HMOX1_gene_expression_in_cerebral_malaria_patients_/515099", "title"=>"Haplotypic quantitative trait analysis of <i>HMOX1</i> gene expression in cerebral malaria patients.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-16 01:24:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/844806"], "description"=>"<p>Abbreviations: CM, cerebral malaria; SnC, severe no cerebral malaria; UM, uncomplicated malaria; UIF, uninfected; RA, reference allele. P-values and Odds Ratios were obtained by logistic regression analysis. Allele frequencies refer to the reference allele conferring susceptibility or resistance to CM.</p>", "links"=>[], "tags"=>["cerebral", "malaria", "single-nucleotide", "polymorphisms", "genotyped"], "article_id"=>515244, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_results_for_cerebral_malaria_risk_single_nucleotide_polymorphisms_SNPs_genotyped_in_TGFB2_CD36_HBB_and_HMOX1_genes_/515244", "title"=>"Association results for cerebral malaria risk single-nucleotide polymorphisms (SNPs) genotyped in <i>TGFB2</i>, <i>CD36</i>, <i>HBB</i> and <i>HMOX1</i> genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-16 01:27:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/844502"], "description"=>"<p>The diagram represents in the vertical axis, the log10 of the P value of association tests of SNPs listed in the y-axis, obtained from logistic regression analysis. The points in red, blue and green represent the results of the association with the SNPs between cases of cerebral malaria (CM) and controls with severe no cerebral malaria (SnC), uncomplicated malaria (UM) and uninfected (UIF), respectively. The upper diagram shows a scale representation of the structure of the <i>HMOX1</i> gene: exons are represented by boxes and marked with its number. The bottom of the diagram represents the LD between a pair of SNPs measured by r<sup>2</sup>. The image, below and to the left, corresponds to the color scale representing the values of LD, from yellow (r<sup>2</sup> = 0) to red (r<sup>2</sup> = 1). This diagram is an adaptation of the figure produced by the snp. plotter R package.</p>", "links"=>[], "tags"=>["ld", "single-nucleotide", "polymorphisms"], "article_id"=>514948, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_tests_and_LD_analysis_in_the_HMOX1_gene_single_nucleotide_polymorphisms_SNPs_/514948", "title"=>"Association tests and LD analysis in the <i>HMOX1</i> gene single-nucleotide polymorphisms (SNPs).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-16 01:22:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/844599"], "description"=>"<p>*Low frequency in the mother-descendent pairs precluded the analysis. Abbreviations: CM, cerebral malaria; SnC, severe no cerebral; Var (O-E), variance (observed-expected).</p>", "links"=>[], "tags"=>["disequilibrium", "haplotypes", "dbsnp"], "article_id"=>515043, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.t004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transmission_disequilibrium_tests_for_associated_TGFB2_and_HMOX1_haplotypes_and_dbSNP_rs334_/515043", "title"=>"Transmission disequilibrium tests for associated <i>TGFB2</i> and <i>HMOX1</i> haplotypes and dbSNP rs334.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-16 01:24:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/844356"], "description"=>"<p>The diagram represents in the vertical axis, the log10 of the P value of association tests of SNPs listed in the y-axis, obtained from logistic regression analysis. The points in red, blue and green represent the results of the association with the SNPs between cases of cerebral malaria (CM) and controls with severe no cerebral malaria (SnC), uncomplicated malaria (UM) and uninfected (UIF), respectively. The upper diagram shows a scale representation of the structure of the <i>TGFB2</i> gene: exons are represented by boxes and marked with its number. The bottom of the diagram represents the LD between a pair of SNPs measured by r<sup>2</sup>. The image, below and to the left, corresponds to the color scale representing the values of LD, from yellow (r<sup>2</sup> = 0) to red (r<sup>2</sup> = 1). This diagram is an adaptation of the figure produced by the snp. plotter R package.</p>", "links"=>[], "tags"=>["ld", "single-nucleotide", "polymorphisms"], "article_id"=>514799, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_tests_and_LD_analysis_in_the_TGFB2_gene_single_nucleotide_polymorphisms_SNPs_/514799", "title"=>"Association tests and LD analysis in the <i>TGFB2</i> gene single-nucleotide polymorphisms (SNPs).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-16 01:19:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/844759"], "description"=>"<p>Abbreviations: CM, cerebral malaria; SnC, severe no cerebral malaria; UM, uncomplicated malaria; UIF, uninfected. Hap-Score represents susceptibility (positive values) or resistance (negative values). In each haplotype are sequentially represented the alleles from SNPs of the LD block: rs2071748, rs8139532, rs7285877, rs11912889 and rs9622194. a) Global Score Statistics Corrected P = 0.06; b) P = 0.009; c) P = 0.10.</p>", "links"=>[], "tags"=>["neurological disorders", "genetics and genomics/genetics of disease", "infectious diseases/protozoal infections"], "article_id"=>515197, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.t003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_results_for_HMOX1_haplotypes_/515197", "title"=>"Association results for <i>HMOX1</i> haplotypes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-16 01:26:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/844704"], "description"=>"<p>Abbreviations: CM, cerebral malaria; SnC, severe no cerebral malaria; UM, uncomplicated malaria; UIF, uninfected. Hap-Score represents susceptibility (positive values) or resistance (negative values). In each haplotype are sequentially represented the alleles from SNPs of the LD block: rs1934852, rs6657275, rs6671370, rs1342586, rs4846478, rs6684205, rs1418553, rs900 and rs1473527. Haplotypes represented have frequency >5% in UIF. Global Score Statistics Corrected P: a) 0.041; b) 0.26; c) 0.41.</p>", "links"=>[], "tags"=>["neurological disorders", "genetics and genomics/genetics of disease", "infectious diseases/protozoal infections"], "article_id"=>515140, "categories"=>["Physics", "Neuroscience", "Genetics"], "users"=>["Maria Rosário Sambo", "Maria Jesus Trovoada", "Carla Benchimol", "Vatúsia Quinhentos", "Lígia Gonçalves", "Rute Velosa", "Maria Isabel Marques", "Nuno Sepulveda", "Taane G. Clark", "Stefan Mustafa", "Oswald Wagner", "António Coutinho", "Carlos Penha-Gonçalves"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011141.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_results_for_TGFB2_haplotypes_/515140", "title"=>"Association results for <i>TGFB2</i> haplotypes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-16 01:25:40"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
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  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"3", "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"=>"11"}
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  • {"unique-ip"=>"6", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
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  • {"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"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"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"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"1", "full-text"=>"1", "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"=>"7", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
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  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
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  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
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  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
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Relative Metric

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