Choriodecidual Infection Downregulates Angiogenesis and Morphogenesis Pathways in Fetal Lungs from Macaca Nemestrina
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{"title"=>"Choriodecidual Infection Downregulates Angiogenesis and Morphogenesis Pathways in Fetal Lungs from Macaca Nemestrina", "type"=>"journal", "authors"=>[{"first_name"=>"Ryan M.", "last_name"=>"McAdams", "scopus_author_id"=>"9843676000"}, {"first_name"=>"Jeroen", "last_name"=>"Vanderhoeven", "scopus_author_id"=>"6602430768"}, {"first_name"=>"Richard P.", "last_name"=>"Beyer", "scopus_author_id"=>"7103099753"}, {"first_name"=>"Theo K.", "last_name"=>"Bammler", "scopus_author_id"=>"35236428200"}, {"first_name"=>"Federico M.", "last_name"=>"Farin", "scopus_author_id"=>"35392146000"}, {"first_name"=>"H. Denny", "last_name"=>"Liggitt", "scopus_author_id"=>"35463082000"}, {"first_name"=>"Raj P.", "last_name"=>"Kapur", "scopus_author_id"=>"26643388300"}, {"first_name"=>"Michael G.", "last_name"=>"Gravett", "scopus_author_id"=>"7004495175"}, {"first_name"=>"Craig E.", "last_name"=>"Rubens", "scopus_author_id"=>"35768373700"}, {"first_name"=>"Kristina M.", "last_name"=>"Adams Waldorf", "scopus_author_id"=>"24437868500"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"365821982", "pmid"=>"23056493", "scopus"=>"2-s2.0-84867283433", "sgr"=>"84867283433", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0046863"}, "id"=>"3eb680e3-7b48-3f89-9196-6026d1bd95c3", "abstract"=>"BACKGROUND: Intrauterine exposure to amniotic fluid (AF) cytokines is thought to predispose to bronchopulmonary dysplasia (BPD). We evaluated the effects of GBS exposure on RNA expression in fetal lung tissue to determine early molecular pathways associated with fetal lung injury that may progress to BPD.\\n\\nMETHODS: Ten chronically catheterized pregnant monkeys (Macaca nemestrina) at 118-125 days gestation (term = 172 days) received choriodecidual inoculation of either: 1) Group B Streptococcus (n = 5) or 2) saline (n = 5). Cesarean section and fetal necropsy was performed in the first week after GBS or saline inoculation regardless of labor. RNA was extracted from fetal lungs and profiled by microarray. Results were analyzed using single gene, Gene Set, and Ingenuity Pathway Analysis. Validation was by RT-PCR and immunohistochemistry.\\n\\nRESULTS: Despite uterine quiescence in most cases, fetal lung injury occurred in four GBS cases (intra-alveolar neutrophils, interstitial thickening) and one control (peri-mortem hemorrhage). Significant elevations of AF cytokines (TNF-α, IL-8, IL-1β, IL-6) were detected in GBS versus controls (p<0.05). Lung injury was not directly caused by GBS, because GBS was undetectable by culture and PCR in the AF and fetal lungs. A total of 335 genes were differentially expressed greater than 1.5 fold (p<0.05) with GBS exposure associated with a striking upregulation of genes in innate and adaptive immunity and downregulation of pathways for angiogenesis, morphogenesis, and cellular growth and development.\\n\\nCONCLUSIONS: A transient choriodecidual infection may induce fetal lung injury with profound alterations in the genetic program of the fetal lung before signs of preterm labor. Our results provide a window for the first time into early molecular pathways disrupting fetal lung angiogenesis and morphogenesis before preterm labor occurs, which may set the stage for BPD. A strategy to prevent BPD should target the fetus in utero to attenuate alterations in the fetal lung genetic program.", "link"=>"http://www.mendeley.com/research/choriodecidual-infection-downregulates-angiogenesis-morphogenesis-pathways-fetal-lungs-macaca-nemest", "reader_count"=>9, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>4, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>1, "Student > Master"=>4, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Medicine and Dentistry"=>4, "Agricultural and Biological Sciences"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/562200"], "description"=>"*<p>Serial cultures of amniotic fluid were tested during the course of the experiment with approximately 10 samples tested per animal. Quantitative real-time PCR was performed on serially sampled amniotic fluid at three points in the course of the experiment including the day prior to inoculation, day of Cesarean section and once during the course of the experiment.</p>", "links"=>[], "tags"=>["fetal", "amniotic"], "article_id"=>232688, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_between_fetal_lung_score_amniotic_fluid_and_fetal_cytokines_culture_results_and_labor_/232688", "title"=>"Correlation between fetal lung score, amniotic fluid and fetal cytokines, culture results and labor.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-09 00:44:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/561984"], "description"=>"<p>First, bacteria from the vagina traffics into the choriodecidual space. Inflammation (e.g. IL-8) is produced by the decidua and/or membranes, which diffuses into the amniotic fluid and fetal lung. Fetal lung injury is induced by inflammatory mediators with significant genes shown involved in inflammation, cellular growth, and angiogenesis. IL, Interleukin; AF, amniotic fluid.</p>", "links"=>[], "tags"=>["conceptual", "events", "fetal"], "article_id"=>232461, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.g005", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Our_conceptual_model_of_events_leading_to_fetal_lung_injury_in_utero_/232461", "title"=>"Our conceptual model of events leading to fetal lung injury <i>in utero</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-09 00:41:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/561852"], "description"=>"<p>Genes shown were filtered for interactions reported in humans only and presented by cellular localization. Direct and indirect interactions are shown by solid lines and dashed lines respectively. Green indicates gene downregulation and red depicts upregulation. White symbols indicate functionally associated neighboring genes that were not differentially expressed in the data. Color intensity represents the average of log2 fold change with brighter colors representing a more significant difference between GBS and controls. Symbols for each molecule are presented according to molecular functions and type of interactions.</p>", "links"=>[], "tags"=>["diagrams", "generated", "neutrophil", "chemotaxis", "ontology", "transcription", "activated"], "article_id"=>232326, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IPA_diagrams_were_generated_for_A_neutrophil_chemotaxis_Gene_Ontology_gene_set_and_B_NF_954_B_a_transcription_factor_predicted_to_be_activated_by_IPA_/232326", "title"=>"IPA diagrams were generated for A) neutrophil chemotaxis Gene Ontology gene set and B) NF-κB, a transcription factor predicted to be activated by IPA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-09 00:38:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/561714"], "description"=>"<p>The x-axis represents individual genes and the y-axis fold-change in expression by either microarray (gray bars) or RT-PCR (black bars). All genes shown were significant in the unadjusted microarray analysis. Genes that were significantly up- or downregulated by RT-PCR between GBS and controls are indicated by a star (two-sided t-test, p<0.05).</p>", "links"=>[], "tags"=>["microarray", "qrt-pcr"], "article_id"=>232199, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_the_microarray_and_qRT_PCR_analysis_/232199", "title"=>"Comparison of the microarray and qRT-PCR analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-09 00:36:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/562333"], "description"=>"*<p>The Functional Analysis of a Network identified biological functions and/or diseases that were most significant to the molecules in the network using a right-tailed Fisher’s exact test.</p>**<p>Canonical Pathway Analysis identified pathways from the IPA library that were most significant to the data set. Significance of the association was measured in two ways: (1) as the ratio of the number of molecules from the focus gene set that map to the pathway to the total number of molecules that map to the canonical pathway and (2) using Fisher’s exact test.</p>***<p>Transcription factor analysis is based on prior knowledge of expected effects between transcription factors and their target genes stored in the IPA library. The overlap p-value measures whether there is a statistically significant overlap between the dataset genes and the genes regulated by a transcription factor using Fisher’s Exact Test.</p>", "links"=>[], "tags"=>["pathway"], "article_id"=>232820, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.t005", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ingenuity_Pathway_Analysis_Summary_/232820", "title"=>"Ingenuity Pathway Analysis Summary.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-09 00:47:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/561564"], "description"=>"<p>Heatmaps of Gene Ontology gene sets associated with A) inflammation, B) angiogenesis and vasculogenesis, and C) morphogenesis and cellular development pathways.</p>", "links"=>[], "tags"=>["ontology", "sets", "angiogenesis", "morphogenesis", "cellular"], "article_id"=>232047, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heatmaps_of_Gene_Ontology_gene_sets_associated_with_A_inflammation_B_angiogenesis_and_vasculogenesis_and_C_morphogenesis_and_cellular_development_pathways_/232047", "title"=>"Heatmaps of Gene Ontology gene sets associated with A) inflammation, B) angiogenesis and vasculogenesis, and C) morphogenesis and cellular development pathways.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-09 00:34:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/562297"], "description"=>"<p>Examples of most differentially regulated single genes.</p>", "links"=>[], "tags"=>["differentially", "regulated"], "article_id"=>232784, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.t002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_most_differentially_regulated_single_genes_/232784", "title"=>"Examples of most differentially regulated single genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-09 00:46:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/562381"], "description"=>"<p>Gene sets downregulated after GBS exposure relative to the control group.</p>", "links"=>[], "tags"=>["sets", "downregulated", "gbs"], "article_id"=>232860, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.t004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_sets_downregulated_after_GBS_exposure_relative_to_the_control_group_/232860", "title"=>"Gene sets downregulated after GBS exposure relative to the control group.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-09 00:47:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/561326"], "description"=>"<p>Panels show hematoxylin and eosin staining (A, B), Leder staining for neutrophils (C, D), CD68 staining for macrophages (E, F), and Masson’s Trichrome staining for collagen (G, H).</p>", "links"=>[], "tags"=>["fetal", "lungs", "shown", "saline", "gbs"], "article_id"=>231809, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.g001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Histopathology_of_the_fetal_lungs_are_shown_on_the_left_for_a_saline_control_with_lung_score_of_0_A_C_E_G_and_on_the_right_for_a_GBS_animal_with_severe_fetal_lung_injury_and_lung_score_of_4_B_D_F_H_/231809", "title"=>"Histopathology of the fetal lungs are shown on the left for a saline control with lung score of 0 (A, C, E, G) and on the right for a GBS animal with severe fetal lung injury and lung score of 4 (B, D, F, H).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-09 00:30:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/297883", "https://ndownloader.figshare.com/files/297921", "https://ndownloader.figshare.com/files/297929", "https://ndownloader.figshare.com/files/297938"], "description"=>"<div><h3>Background</h3><p>Intrauterine exposure to amniotic fluid (AF) cytokines is thought to predispose to bronchopulmonary dysplasia (BPD). We evaluated the effects of GBS exposure on RNA expression in fetal lung tissue to determine early molecular pathways associated with fetal lung injury that may progress to BPD.</p> <h3>Methods</h3><p>Ten chronically catheterized pregnant monkeys (<em>Macaca nemestrina</em>) at 118–125 days gestation (term = 172 days) received choriodecidual inoculation of either: 1) Group B Streptococcus (n = 5) or 2) saline (n = 5). Cesarean section and fetal necropsy was performed in the first week after GBS or saline inoculation regardless of labor. RNA was extracted from fetal lungs and profiled by microarray. Results were analyzed using single gene, Gene Set, and Ingenuity Pathway Analysis. Validation was by RT-PCR and immunohistochemistry.</p> <h3>Results</h3><p>Despite uterine quiescence in most cases, fetal lung injury occurred in four GBS cases (intra-alveolar neutrophils, interstitial thickening) and one control (peri-mortem hemorrhage). Significant elevations of AF cytokines (TNF-α, IL-8, IL-1β, IL-6) were detected in GBS versus controls (p<0.05). Lung injury was not directly caused by GBS, because GBS was undetectable by culture and PCR in the AF and fetal lungs. A total of 335 genes were differentially expressed greater than 1.5 fold (p<0.05) with GBS exposure associated with a striking upregulation of genes in innate and adaptive immunity and downregulation of pathways for angiogenesis, morphogenesis, and cellular growth and development.</p> <h3>Conclusions</h3><p>A transient choriodecidual infection may induce fetal lung injury with profound alterations in the genetic program of the fetal lung before signs of preterm labor. Our results provide a window for the first time into early molecular pathways disrupting fetal lung angiogenesis and morphogenesis before preterm labor occurs, which may set the stage for BPD. A strategy to prevent BPD should target the fetus <em>in utero</em> to attenuate alterations in the fetal lung genetic program.</p> </div>", "links"=>[], "tags"=>["choriodecidual", "downregulates", "angiogenesis", "morphogenesis", "pathways", "fetal", "lungs"], "article_id"=>118724, "categories"=>["Medicine", "Cancer", "Microbiology", "Immunology", "Physiology"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0046863.s001", "https://dx.doi.org/10.1371/journal.pone.0046863.s002", "https://dx.doi.org/10.1371/journal.pone.0046863.s003", "https://dx.doi.org/10.1371/journal.pone.0046863.s004"], "stats"=>{"downloads"=>16, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Choriodecidual_Infection_Downregulates_Angiogenesis_and_Morphogenesis_Pathways_in_Fetal_Lungs_from_Macaca_Nemestrina_/118724", "title"=>"Choriodecidual Infection Downregulates Angiogenesis and Morphogenesis Pathways in Fetal Lungs from <em>Macaca Nemestrina</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-10-09 02:25:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/562251"], "description"=>"<p>Gene sets upregulated after GBS exposure relative to the control group.</p>", "links"=>[], "tags"=>["sets", "upregulated", "gbs"], "article_id"=>232737, "categories"=>["Medicine", "Microbiology", "Virology", "Physiology", "Immunology", "Infectious Diseases"], "users"=>["Ryan M. McAdams", "Jeroen Vanderhoeven", "Richard P. Beyer", "Theo K. Bammler", "Federico M. Farin", "H. Denny Liggitt", "Raj P. Kapur", "Michael G. Gravett", "Craig E. Rubens", "Kristina M. Adams Waldorf"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046863.t003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_sets_upregulated_after_GBS_exposure_relative_to_the_control_group_/232737", "title"=>"Gene sets upregulated after GBS exposure relative to the control group.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-09 00:45:37"}

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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"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"=>"4"}
  • {"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"=>"2017", "month"=>"5"}
  • {"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"=>"6"}
  • {"unique-ip"=>"2", "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"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"13", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"10", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2017", "month"=>"10"}

Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[319, 556, 679, 785, 881, 970, 1062, 1149, 1236, 1323, 1402, 1474, 1545, 1617, 1681, 1754, 1822, 1892, 1963, 2031, 2099, 2165, 2233, 2299, 2359]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[313, 562, 690, 796, 893, 986, 1079, 1173, 1257, 1349, 1429, 1506, 1586, 1661, 1730, 1803, 1876, 1945, 2017, 2091, 2163, 2225, 2294, 2362, 2430]}, {"subject_area"=>"/Biology and life sciences/Immunology", "average_usage"=>[312, 555, 680, 785, 880, 965, 1057, 1142, 1230, 1312, 1394, 1471, 1547, 1613, 1681, 1743, 1805, 1871, 1941, 2010, 2071, 2128, 2202, 2266, 2323]}, {"subject_area"=>"/Biology and life sciences/Physiology", "average_usage"=>[307, 536, 653, 753, 839, 926, 1017, 1103, 1189, 1268, 1348, 1425, 1492, 1557, 1620, 1686, 1759, 1825, 1891, 1950, 2014, 2079, 2141, 2200, 2255]}, {"subject_area"=>"/Medicine and health sciences/Physiology", "average_usage"=>[308, 535, 653, 754, 847, 930, 1020, 1103, 1188, 1268, 1351, 1420, 1487, 1550, 1614, 1679, 1757, 1830, 1898, 1961, 2024, 2086, 2150, 2216, 2266]}]}
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