Glucose- but Not Rice-Based Oral Rehydration Therapy Enhances the Production of Virulence Determinants in the Human Pathogen Vibrio cholerae
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{"title"=>"Glucose- but Not Rice-Based Oral Rehydration Therapy Enhances the Production of Virulence Determinants in the Human Pathogen Vibrio cholerae", "type"=>"journal", "authors"=>[{"first_name"=>"Juliane", "last_name"=>"Kühn", "scopus_author_id"=>"56602285300"}, {"first_name"=>"Flavio", "last_name"=>"Finger", "scopus_author_id"=>"56190321600"}, {"first_name"=>"Enrico", "last_name"=>"Bertuzzo", "scopus_author_id"=>"23972622800"}, {"first_name"=>"Sandrine", "last_name"=>"Borgeaud", "scopus_author_id"=>"55552392500"}, {"first_name"=>"Marino", "last_name"=>"Gatto", "scopus_author_id"=>"7006490979"}, {"first_name"=>"Andrea", "last_name"=>"Rinaldo", "scopus_author_id"=>"7103192491"}, {"first_name"=>"Melanie", "last_name"=>"Blokesch", "scopus_author_id"=>"6507156426"}], "year"=>2014, "source"=>"PLoS Neglected Tropical Diseases", "identifiers"=>{"scopus"=>"2-s2.0-84928237151", "sgr"=>"84928237151", "issn"=>"19352735", "isbn"=>"1935-2735", "pmid"=>"25474211", "doi"=>"10.1371/journal.pntd.0003347", "pui"=>"603940737"}, "id"=>"51ee99a2-58c0-347d-8104-efefbc482e49", "abstract"=>"Despite major attempts to prevent cholera transmission, millions of people worldwide still must address this devastating disease. Cholera research has so far mainly focused on the causative agent, the bacterium Vibrio cholerae, or on disease treatment, but rarely were results from both fields interconnected. Indeed, the treatment of this severe diarrheal disease is mostly accomplished by oral rehydration therapy (ORT), whereby water and electrolytes are replenished. Commonly distributed oral rehydration salts also contain glucose. Here, we analyzed the effects of glucose and alternative carbon sources on the production of virulence determinants in the causative agent of cholera, the bacterium Vibrio cholerae during in vitro experimentation. We demonstrate that virulence gene expression and the production of cholera toxin are enhanced in the presence of glucose or similarly transported sugars in a ToxR-, TcpP- and ToxT-dependent manner. The virulence genes were significantly less expressed if alternative non-PTS carbon sources, including rice-based starch, were utilized. Notably, even though glucose-based ORT is commonly used, field studies indicated that rice-based ORT performs better. We therefore used a spatially explicit epidemiological model to demonstrate that the better performing rice-based ORT could have a significant impact on epidemic progression based on the recent outbreak of cholera in Haiti. Our results strongly support a change of carbon source for the treatment of cholera, especially in epidemic settings.", "link"=>"http://www.mendeley.com/research/glucose-not-ricebased-oral-rehydration-therapy-enhances-production-virulence-determinants-human-path-2", "reader_count"=>16, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>2, "Student > Master"=>4, "Student > Bachelor"=>5}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>2, "Student > Master"=>4, "Student > Bachelor"=>5}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Environmental Science"=>1, "Nursing and Health Professions"=>2, "Agricultural and Biological Sciences"=>5, "Medicine and Dentistry"=>6, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Spain"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1821349"], "description"=>"<p>Upon virulence-inducing conditions (e.g., in the human intestine or by <i>in vitro</i> provision of bicarbonate as inducer <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003347#pntd.0003347-Nielsen1\" target=\"_blank\">[21]</a>, <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003347#pntd.0003347-Abuaita1\" target=\"_blank\">[29]</a>) the human pathogen <i>V. cholerae</i> expresses amongst others the virulence genes of the <i>tcp</i> and <i>ctx</i> clusters, which ultimately leads to the synthesis and assembly of the toxin-coregulated pilus (TCP) and the production of cholera toxin, respectively. The TCP forms a type IV pilus structure on the bacterial surface, which is required for intestinal colonization. The cholera toxin indirectly leads to efflux of ions (concomitantly with water), which causes the dramatic watery diarrhea, the hallmark of cholera. In this study, we assessed the expression of the <i>tcp</i> and <i>ctx</i> genes and the production of cholera toxin under virulence-inducing conditions and in the presence of diverse carbon sources. Our data indicate that glucose strongly enhances the virulence potential of the pathogen (indicated by the arrows). Thus, based on the better performance of rice-based ORT as described in field studies and on our model-guided prediction of cholera transmission under epidemic settings we suggest that rice-based ORT should be reconsidered for the treatment of cholera.</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260028, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glucose_based_oral_rehydration_therapy_ORT_might_enhance_the_production_of_virulence_determinates_in_V_cholerae_thereby_extending_the_duration_of_the_disease_and_worsen_the_symptoms_compared_to_rice_based_ORT_/1260028", "title"=>"Glucose-based oral rehydration therapy (ORT) might enhance the production of virulence determinates in <i>V. cholerae</i> thereby extending the duration of the disease and worsen the symptoms compared to rice-based ORT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821352"], "description"=>"<p>(<b>A</b>) Relative expression of virulence-associated genes in the <i>V. cholerae</i> wild-type strain A1552. The virulence inducer bicarbonate was present in all samples. Supplemented carbon sources were lactate and glucose as indicated by the white and black columns, respectively. Statistics were applied using Student's t-test (**, <i>P</i>≤0.01; ***, <i>P</i>≤0.001). (<b>B</b>) Quantification of cholera toxin that was produced upon growth on diverse carbon sources (as indicated). The data were normalized by the OD<sub>600</sub> values of the bacterial culture. For rice starch-grown cells the OD<sub>600</sub> value was deduced from the number of counted bacteria. All data represent averages from three independent biological experiments ± SD.</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260031, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_and_production_of_virulence_factors_in_V_cholerae_is_enhanced_in_the_presence_of_glucose_/1260031", "title"=>"Expression and production of virulence factors in <i>V. cholerae</i> is enhanced in the presence of glucose.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821353"], "description"=>"<p>(<b>A</b>) Simplified overview of the regulatory cascade that is involved in virulence gene expression in <i>V. cholerae</i>. <i>toxT</i> expression occurs upon activation by the regulatory proteins ToxR and TcpP (complexed with ToxS and TcpH, respectively) as indicated by the arrows (solid lines). Next, the synthesized ToxT protein (dashed arrow) induces the expression of the <i>tcp</i> cluster and the <i>ctxAB</i> operon, which ultimately leads to the production of TCP and CT. Elements acting upstream <i>tcpPH</i> and <i>toxRS</i> are excluded for sake of simplicity. Scheme is based on <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003347#pntd.0003347-Matson1\" target=\"_blank\">[13]</a>. (<b>B+C</b>) Relative expression of the genes <i>tcpA, tcpB, ctxA</i>, and <i>ctxB</i> in diverse <i>V. cholerae</i> strains, which were grown under virulence-inducing conditions in the presence of lactate (lac) or glucose (glc). Strains tested as indicated above the graphs: panel B: wild type <i>V. cholerae</i> strain (WT; A1552-Tn<i>tfoX</i>) and its <i>toxR</i> and <i>tcpP</i>-negative derivatives (ΔtoxR and ΔtcpP). panel C: wild type (WT; A1552) and ΔtoxT (A1552ΔtoxT). (<b>D</b>) As in panels B and C except that the <i>V. cholerae</i> wild-type strain was grown under glucose-containing virulence-inducing conditions in the presence of DMSO (gray bars) or virstatin (50 µM dissolved in DMSO; red bars). The values shown in panels B, C, and D represent averages of at least three independent biological replicates (± SD) Statistics were applied on pairwise comparisons using Student's t-test (ns, non-significant; *, <i>P</i>≤0.05; **, <i>P</i>≤0.01; ***, <i>P</i>≤0.001).</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260032, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_virulence_determinants_is_dependent_on_the_common_virulence_regulators_under_in_vitro_conditions_/1260032", "title"=>"Expression of virulence determinants is dependent on the common virulence regulators under <i>in vitro</i> conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821358"], "description"=>"<p>Bacterial cultures were induced for virulence in the presence of glucose for 30 min, washed (where indicated) and shifted to virulence-non-inducing or virulence-inducing medium containing either glucose or starch. The amount of CT was determined as described for <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003347#pntd-0003347-g002\" target=\"_blank\">Figure 2</a>. Statistically significant differences were determined through Student's t-test (* <i>P</i>≤0.05).</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260035, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Shifting_V_cholerae_from_glucose_based_to_starch_based_conditions_leads_to_a_decrease_in_CT_production_/1260035", "title"=>"Shifting <i>V. cholerae</i> from glucose-based to starch-based conditions leads to a decrease in CT production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821368"], "description"=>"<p>(<b>A</b>) Computational subunits of Haiti with population sizes. Each unit corresponds to one node in our model. (<b>B</b>) Evolution of the epidemic over time for the entire country. Observed cases (grey bars), calibrated model (dark blue), and model runs with a ten percent reduction of symptomatic shedding rate as well as disease duration due to rice-based ORT (light blue). Shaded areas show the 95% confidence intervals resulting from parameter uncertainty; the solid lines show the median trajectory. The replacement of glucose-based with rice-based ORT was assumed to take place 30 days after the onset of the epidemic. (<b>C</b>) Evolution of the epidemics based on shedding rate and disease duration. Contour plot of the percentage of total cases in the whole country until December 2011, predicted by the model when applying variable reductions of the shedding rate (y-axis) and disease duration (x-axis), compared to the cases predicted by the calibrated model.</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260041, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modeling_the_effect_of_rice_based_ORT_on_the_Haitian_cholera_outbreak_/1260041", "title"=>"Modeling the effect of rice-based ORT on the Haitian cholera outbreak.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821370"], "description"=>"<p>Virulence gene expression in <i>V. cholerae</i> cultures that were grown in the presence of 50 mM glucose (glc) compared with cells that were grown with the indicated carbon sources. The fold differences are indicated. GlcNAc, N-acetylglucosamine.</p><p>Transcript levels of virulence factor encoding genes in the presence of different carbon sources.</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260043, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcript_levels_of_virulence_factor_encoding_genes_in_the_presence_of_different_carbon_sources_/1260043", "title"=>"Transcript levels of virulence factor encoding genes in the presence of different carbon sources.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821372"], "description"=>"<p>Bacterial cultures contained the indicated carbon sources (glucose, GlcNAc, sucrose) plus lactate to maintain growth. Strains tested for the expression of the indicated genes (relative to the housekeeping gene <i>gyrA</i>) were: wild-type (WT), and the respective PTS mutants for glucose (ΔptsG), GlcNAc (ΔnagE), and sucrose (ΔscrA) in the absence (−) or presence (+) of bicarbonate as virulence inducer. Average of at least three independent experiments (± SD) are depicted. Statistics were applied using Student's t-test comparing the WT (+) and Δpts (+) conditions (* <i>P</i>≤0.05; ** <i>P</i>≤0.01; *** <i>P</i>≤0.001; <i>ns</i>, not statistically different).</p><p>PTS sugar-dependent virulence gene expression requires sugar uptake.</p>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260045, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PTS_sugar_dependent_virulence_gene_expression_requires_sugar_uptake_/1260045", "title"=>"PTS sugar-dependent virulence gene expression requires sugar uptake.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-04 03:02:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1821415", "https://ndownloader.figshare.com/files/1821416", "https://ndownloader.figshare.com/files/1821418", "https://ndownloader.figshare.com/files/1821419", "https://ndownloader.figshare.com/files/1821420", "https://ndownloader.figshare.com/files/1821421", "https://ndownloader.figshare.com/files/1821422", "https://ndownloader.figshare.com/files/1821423", "https://ndownloader.figshare.com/files/1821424", "https://ndownloader.figshare.com/files/1821426", "https://ndownloader.figshare.com/files/1821427", "https://ndownloader.figshare.com/files/1821428", "https://ndownloader.figshare.com/files/1821429"], "description"=>"<div><p>Despite major attempts to prevent cholera transmission, millions of people worldwide still must address this devastating disease. Cholera research has so far mainly focused on the causative agent, the bacterium <i>Vibrio cholerae</i>, or on disease treatment, but rarely were results from both fields interconnected. Indeed, the treatment of this severe diarrheal disease is mostly accomplished by oral rehydration therapy (ORT), whereby water and electrolytes are replenished. Commonly distributed oral rehydration salts also contain glucose. Here, we analyzed the effects of glucose and alternative carbon sources on the production of virulence determinants in the causative agent of cholera, the bacterium <i>Vibrio cholerae</i> during <i>in vitro</i> experimentation. We demonstrate that virulence gene expression and the production of cholera toxin are enhanced in the presence of glucose or similarly transported sugars in a ToxR-, TcpP- and ToxT-dependent manner. The virulence genes were significantly less expressed if alternative non-PTS carbon sources, including rice-based starch, were utilized. Notably, even though glucose-based ORT is commonly used, field studies indicated that rice-based ORT performs better. We therefore used a spatially explicit epidemiological model to demonstrate that the better performing rice-based ORT could have a significant impact on epidemic progression based on the recent outbreak of cholera in Haiti. Our results strongly support a change of carbon source for the treatment of cholera, especially in epidemic settings.</p></div>", "links"=>[], "tags"=>["alternative carbon sources", "virulence determinants", "disease treatment", "cholera toxin", "ort", "Cholera research", "Human Pathogen Vibrio cholerae", "diarrheal disease", "virulence genes", "epidemic progression", "rehydration salts", "carbon source", "virulence gene expression", "cholera transmission", "epidemic settings", "rehydration therapy", "field studies", "glucose", "agent", "bacterium Vibrio cholerae"], "article_id"=>1260074, "categories"=>["Uncategorised"], "users"=>["Juliane Kühn", "Flavio Finger", "Enrico Bertuzzo", "Sandrine Borgeaud", "Marino Gatto", "Andrea Rinaldo", "Melanie Blokesch"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0003347.s001", "https://dx.doi.org/10.1371/journal.pntd.0003347.s002", "https://dx.doi.org/10.1371/journal.pntd.0003347.s003", "https://dx.doi.org/10.1371/journal.pntd.0003347.s004", "https://dx.doi.org/10.1371/journal.pntd.0003347.s005", "https://dx.doi.org/10.1371/journal.pntd.0003347.s006", "https://dx.doi.org/10.1371/journal.pntd.0003347.s007", "https://dx.doi.org/10.1371/journal.pntd.0003347.s008", "https://dx.doi.org/10.1371/journal.pntd.0003347.s009", "https://dx.doi.org/10.1371/journal.pntd.0003347.s010", "https://dx.doi.org/10.1371/journal.pntd.0003347.s011", "https://dx.doi.org/10.1371/journal.pntd.0003347.s012", "https://dx.doi.org/10.1371/journal.pntd.0003347.s013"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Glucose_but_Not_Rice_Based_Oral_Rehydration_Therapy_Enhances_the_Production_of_Virulence_Determinants_in_the_Human_Pathogen_Vibrio_cholerae_/1260074", "title"=>"Glucose- but Not Rice-Based Oral Rehydration Therapy Enhances the Production of Virulence Determinants in the Human Pathogen <i>Vibrio cholerae</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-04 03:02:22"}

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  • {"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"=>"2018", "month"=>"2"}
  • {"unique-ip"=>"22", "full-text"=>"21", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"18", "full-text"=>"17", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"9", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"14", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"13", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"14", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "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"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[]}
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