TLR-2 Activation Induces Regulatory T Cells and Long-Term Suppression of Asthma Manifestations in Mice
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{"title"=>"TLR-2 Activation Induces Regulatory T Cells and Long-Term Suppression of Asthma Manifestations in Mice", "type"=>"journal", "authors"=>[{"first_name"=>"Martijn C.", "last_name"=>"Nawijn", "scopus_author_id"=>"6506545287"}, {"first_name"=>"Alexandre C.", "last_name"=>"Motta", "scopus_author_id"=>"8850452800"}, {"first_name"=>"Renée", "last_name"=>"Gras", "scopus_author_id"=>"23100008500"}, {"first_name"=>"Soheila", "last_name"=>"Shirinbak", "scopus_author_id"=>"36614713500"}, {"first_name"=>"Hadi", "last_name"=>"Maazi", "scopus_author_id"=>"36572219400"}, {"first_name"=>"Antoon J.M.", "last_name"=>"van Oosterhout", "scopus_author_id"=>"7006766304"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84873488653", "pmid"=>"23393567", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"368294457", "issn"=>"19326203", "scopus"=>"2-s2.0-84873488653", "doi"=>"10.1371/journal.pone.0055307"}, "id"=>"cfbab91d-0000-353d-bd7c-6680d10fd73e", "abstract"=>"Asthma is a chronic inflammatory disease of the airways characterized by variable airway obstruction and airway hyperresponsiveness (AHR). The T regulatory (Treg) cell subset is critically important for the regulation of immune responses. Adoptive transfer of Treg cells has been shown to be sufficient for the suppression of airway inflammation in experimental allergic asthma. Intervention strategies aimed at expanding the Treg cell population locally in the airways of sensitized individuals are therefore of high interest as a potential therapeutic treatment for allergic airway disease. Here, we aim to test whether long-term suppression of asthma manifestations can be achieved by locally expanding the Treg cell subset via intranasal administration of a TLR-2 agonist. To model therapeutic intervention aimed at expanding the endogenous Treg population in a sensitized host, we challenged OVA-sensitized mice by OVA inhalation with concomitant intranasal instillation of the TLR-2 agonist Pam3Cys, followed by an additional series of OVA challenges. Pam3Cys treatment induced an acute but transient aggravation of asthma manifestations, followed by a reduction or loss of AHR to methacholine, depending on the time between Pam3Cys treatment and OVA challenges. In addition, Pam3Cys-treatment induced significant reductions of eosinophils and increased numbers of Treg cells in the lung infiltrates. Our data show that, despite having adverse acute effects, TLR2 agonist treatment as a therapeutic intervention induces an expansion of the Treg cell population in the lungs and results in long-term protection against manifestation of allergic asthma upon subsequent allergen provocation. Our data indicate that local expansion of Tregs in allergic airway disease is an interesting therapeutic approach that warrants further investigation.", "link"=>"http://www.mendeley.com/research/tlr2-activation-induces-regulatory-t-cells-longterm-suppression-asthma-manifestations-mice", "reader_count"=>31, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>10, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>9, "Medicine and Dentistry"=>7, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemistry"=>1, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>9}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/494838"], "description"=>"<p>Mice (n = 8) were sensitized with OVA/Alum and received a first series of 3 OVA inhalation challenges, during which TLR-2 agonist (20 µg per mouse in PBS) or PBS was administered intranasally 1 hour before challenge. After 3 weeks, mice received a second series of 3 inhalation challenges (OVA or PBS). Asthma manifestations were measured one day after the last challenge. A: Airway responsiveness to increasing doses of methacholine was measured by whole-body plethysmography and is expressed as enhanced pause (PenH) (gray symbols: PBS-challenged groups, white symbols: OVA-challenged groups, squares: Pam3Cys-treated groups, triangles: PBS-treated groups). B: total cell counts in the BAL of PBS and OVA-challenged mice as indicated. C: differential cell counts in the BAL of OVA-challenged mice only. D: OVA-specific IgE levels in pre-challenge and post-challenge sera of OVA-challenged mice. (E) Lung tissue cytokines measured in lung homogenates of PBS or Pam3Cys (P3C) treated mice after OVA challenge at timepoint 1 (left-hand panel) or at timepoint 2 (right-hand panel) as indicated. All values in panels A–D are displayed as average ± SEM, panel E displays individual values (dots)+mean (bar). Significance is indicated (*) when p<0.05.</p>", "links"=>[], "tags"=>["cells", "infiltration", "ova-specific", "ige", "serum"], "article_id"=>165357, "categories"=>["Immunology"], "users"=>["Martijn C. Nawijn", "Alexandre C. Motta", "Renée Gras", "Soheila Shirinbak", "Hadi Maazi", "Antoon J. M. van Oosterhout"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055307.g004", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Airway_responsiveness_lung_cells_infiltration_and_OVA_specific_IgE_serum_levels_/165357", "title"=>"Airway responsiveness, lung cells infiltration and OVA-specific IgE serum levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:55:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/494940"], "description"=>"<p>Total cells in the BAL isolated at both timepoints of protocol 2 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055307#pone-0055307-g001\" target=\"_blank\">Figure 1b</a>) were stained for CD4, CD25 and FoxP3, and analyzed by flowcytometry. A. FACS staining profiles for representative FACS plots of the four groups analyzed at timepoint 2. Forward and Side scatter profiles are used to define lymphocytes, CD4-PerCP/FoxP3-PE was used to identify FoxP3<sup>+</sup> regulatory T cells. (B, C) Number of CD25<sup>+</sup>FoxP3<sup>+</sup> cells is shown as a fraction of the total CD4<sup>+</sup> T cell count. B: the fraction of CD25<sup>+</sup>FoxP3<sup>+</sup> cells within the CD4<sup>+</sup> T cells from lung 24 h after the last of three OVA challenges in the presence or absence of Pam3Cys, as indicated. C: the fraction of CD25<sup>+</sup>FoxP3<sup>+</sup> cells within the CD4<sup>+</sup> T cells from lung 24 h after the last of three OVA or PBS challenges, three weeks after the first series of challenges as depicted in panel A. Treatment at the first series of challenges is indicated on the X-axis. All values are displayed as average ± SEM. Significance is indicated (*) when p<0.05 or (***) when p<0.005.</p>", "links"=>[], "tags"=>["cells"], "article_id"=>165460, "categories"=>["Immunology"], "users"=>["Martijn C. Nawijn", "Alexandre C. Motta", "Renée Gras", "Soheila Shirinbak", "Hadi Maazi", "Antoon J. M. van Oosterhout"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055307.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CD25_FoxP3_CD4_T_cells_in_BAL_/165460", "title"=>"CD25<sup>+</sup>FoxP3<sup>+</sup> CD4<sup>+</sup> T cells in BAL.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:55:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/494591"], "description"=>"<p>Mice (n = 8) were sensitized with OVA/Alum and received 4 OVA or PBS inhalation challenges. TLR-2 agonist (20 µg per mouse in PBS) or PBS was administered intranasally 1 hour before the 2 first challenges. Asthma manifestations were measured one day after the last challenge. A: Airway responsiveness to increasing doses of methacholine was measured by whole-body plethysmography and is expressed as enhanced pause (PenH) (gray symbols: PBS-challenged groups, white symbols: OVA-challenged groups, squares: Pam3Cys-treated groups, triangles: PBS-treated groups). B, C: total (B) and differential (C) cell counts in the BAL of PBS and OVA-challenged mice as indicated. D: OVA-specific IgE levels in the serum of PBS and OVA-challenged mice as indicated. All values are displayed as average ± SEM.</p>", "links"=>[], "tags"=>["bal", "counts", "ova-specific", "ige", "serum"], "article_id"=>165108, "categories"=>["Immunology"], "users"=>["Martijn C. Nawijn", "Alexandre C. Motta", "Renée Gras", "Soheila Shirinbak", "Hadi Maazi", "Antoon J. M. van Oosterhout"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055307.g002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Airway_responsiveness_BAL_cell_counts_and_composition_and_OVA_specific_IgE_serum_levels_/165108", "title"=>"Airway responsiveness, BAL cell counts and composition, and OVA-specific IgE serum levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:53:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/494686"], "description"=>"<p>Mice (n = 8) were sensitized with OVA/Alum and received 3 OVA or PBS inhalation challenges. TLR-2 agonist (20 µg per mouse in PBS) or PBS was administered intranasally 1 hour before each challenge. Asthma manifestations were measured one day after the last challenge. A: Airway responsiveness to increasing doses of methacholine was measured by whole-body plethysmography and is expressed as enhanced pause (PenH) (gray symbols: PBS-challenged groups, white symbols: OVA-challenged groups, squares: Pam3Cys-treated groups, triangles: PBS-treated groups). B, C: total (B) and differential (C) cell counts in the BAL of OVA-challenged mice. D: OVA-specific IgE levels in the serum of OVA-challenged mice. (E) Lung tissue cytokines measured in lung homogenates of PBS or Pam3Cys (P3C) treated mice as indicated. All values are displayed as average ± SEM (panels A–D) or individual values (dots)+mean (bar) (panel E). Significance is indicated (*) when p<0.05.</p>", "links"=>[], "tags"=>["infiltration", "ova-specific", "ige", "serum"], "article_id"=>165201, "categories"=>["Immunology"], "users"=>["Martijn C. Nawijn", "Alexandre C. Motta", "Renée Gras", "Soheila Shirinbak", "Hadi Maazi", "Antoon J. M. van Oosterhout"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055307.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Airway_responsiveness_lung_cell_infiltration_and_OVA_specific_IgE_serum_levels_/165201", "title"=>"Airway responsiveness, lung cell infiltration and OVA-specific IgE serum levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:54:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/494498"], "description"=>"<p>Days of sensitization, OVA/PBS challenges, Pam3Cys/PBS treatments and lung function measurements/section are indicated for both the short protocol (A) and the long-term protocol (B).</p>", "links"=>[], "tags"=>["immunology"], "article_id"=>165007, "categories"=>["Immunology"], "users"=>["Martijn C. Nawijn", "Alexandre C. Motta", "Renée Gras", "Soheila Shirinbak", "Hadi Maazi", "Antoon J. M. van Oosterhout"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055307.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_schedule_of_the_experimental_procedures_/165007", "title"=>"Time schedule of the experimental procedures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:53:15"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"29", "full-text"=>"33", "pdf"=>"16", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"2"}
  • {"unique-ip"=>"31", "full-text"=>"38", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"4"}
  • {"unique-ip"=>"34", "full-text"=>"35", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"6"}
  • {"unique-ip"=>"21", "full-text"=>"24", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"7"}
  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"8"}
  • {"unique-ip"=>"24", "full-text"=>"22", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"22", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"26", "full-text"=>"27", "pdf"=>"20", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"20", "full-text"=>"22", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"10", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"1"}
  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"2"}
  • {"unique-ip"=>"20", "full-text"=>"19", "pdf"=>"11", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"16", "full-text"=>"15", "pdf"=>"9", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"12", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"7", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"5", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"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"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"5", "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"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"4", "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"=>"7", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[275, 472, 605, 720, 822, 921, 1013, 1106, 1200, 1289, 1378, 1459, 1531]}, {"subject_area"=>"/Medicine and health sciences/Anatomy and physiology", "average_usage"=>[253, 430]}, {"subject_area"=>"/Medicine and health sciences/Pulmonology", "average_usage"=>[241, 428, 552, 659, 752, 848, 934, 1028, 1106, 1183, 1267, 1350, 1401]}]}
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