Long-Chain Fatty Acid Combustion Rate Is Associated with Unique Metabolite Profiles in Skeletal Muscle Mitochondria
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{"title"=>"Long-chain fatty acid combustion rate is associated with unique metabolite profiles in skeletal muscle mitochondria", "type"=>"journal", "authors"=>[{"first_name"=>"Erin L.", "last_name"=>"Seifert", "scopus_author_id"=>"15840392200"}, {"first_name"=>"Oliver", "last_name"=>"Fiehn", "scopus_author_id"=>"7003325967"}, {"first_name"=>"Véronic", "last_name"=>"Bezaire", "scopus_author_id"=>"6507729802"}, {"first_name"=>"David R.", "last_name"=>"Bickel", "scopus_author_id"=>"7005738250"}, {"first_name"=>"Gert", "last_name"=>"Wohlgemuth", "scopus_author_id"=>"8908870200"}, {"first_name"=>"Sean H.", "last_name"=>"Adams", "scopus_author_id"=>"7402058156"}, {"first_name"=>"Mary Ellen", "last_name"=>"Harper", "scopus_author_id"=>"7201849148"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"78650735706", "doi"=>"10.1371/journal.pone.0009834", "pui"=>"368277850", "pmid"=>"20352092", "scopus"=>"2-s2.0-78650735706", "issn"=>"19326203", "isbn"=>"1932-6203"}, "id"=>"a05c46c6-e1b3-3bbb-8949-a5cb4c98da1f", "abstract"=>"BACKGROUND/AIM: Incomplete or limited long-chain fatty acid (LCFA) combustion in skeletal muscle has been associated with insulin resistance. Signals that are responsive to shifts in LCFA beta-oxidation rate or degree of intramitochondrial catabolism are hypothesized to regulate second messenger systems downstream of the insulin receptor. Recent evidence supports a causal link between mitochondrial LCFA combustion in skeletal muscle and insulin resistance. We have used unbiased metabolite profiling of mouse muscle mitochondria with the aim of identifying candidate metabolites within or effluxed from mitochondria and that are shifted with LCFA combustion rate.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Large-scale unbiased metabolomics analysis was performed using GC/TOF-MS on buffer and mitochondrial matrix fractions obtained prior to and after 20 min of palmitate catabolism (n = 7 mice/condition). Three palmitate concentrations (2, 9 and 19 microM; corresponding to low, intermediate and high oxidation rates) and 9 microM palmitate plus tricarboxylic acid (TCA) cycle and electron transport chain inhibitors were each tested and compared to zero palmitate control incubations. Paired comparisons of the 0 and 20 min samples were made by Student's t-test. False discovery rate were estimated and Type I error rates assigned. Major metabolite groups were organic acids, amines and amino acids, free fatty acids and sugar phosphates. Palmitate oxidation was associated with unique profiles of metabolites, a subset of which correlated to palmitate oxidation rate. In particular, palmitate oxidation rate was associated with distinct changes in the levels of TCA cycle intermediates within and effluxed from mitochondria.\\n\\nCONCLUSIONS/SIGNIFICANCE: This proof-of-principle study establishes that large-scale metabolomics methods can be applied to organelle-level models to discover metabolite patterns reflective of LCFA combustion, which may lead to identification of molecules linking muscle fat metabolism and insulin signaling. Our results suggest that future studies should focus on the fate of effluxed TCA cycle intermediates and on mechanisms ensuring their replenishment during LCFA metabolism in skeletal muscle.", "link"=>"http://www.mendeley.com/research/longchain-fatty-acid-combustion-rate-associated-unique-metabolite-profiles-skeletal-muscle-mitochond-2", "reader_count"=>20, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>4, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Mathematics"=>1, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>2, "Sports and Recreations"=>3, "Chemistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Mathematics"=>{"Mathematics"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Japan"=>1, "Malaysia"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/857851"], "description"=>"<p>Significance: paired t-test, 0 <i>vs</i>. 20 min, within treatment; * P<0.05; **, P<0.02, *** P<0.005. ‡: indicates that an outlier was removed. See legend to <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009834#pone-0009834-g005\" target=\"_blank\">Figure 5</a> for further details.</p>", "links"=>[], "tags"=>["3-hydroxybutanoic", "buffer", "matrix", "fractions", "mitochondrial"], "article_id"=>528288, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_3_hydroxybutanoic_acid_over_time_in_buffer_and_matrix_fractions_obtained_from_muscle_mitochondrial_preparations_/528288", "title"=>"Changes in 3-hydroxybutanoic acid over time in buffer and matrix fractions obtained from muscle mitochondrial preparations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:18:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/858008"], "description"=>"<p>Condition: concentration of palmitate; inh: inhibitors added.</p>", "links"=>[], "tags"=>["rates", "corresponding", "metabolites", "changed", "20-min", "incubation"], "article_id"=>528451, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimated_false_discovery_rates_FDR_P_value_threshold_paired_t_test_and_corresponding_number_of_metabolites_that_changed_over_the_20_min_incubation_in_each_fraction_matrix_buffer_/528451", "title"=>"Estimated false discovery rates (FDR), P value threshold (paired t-test), and corresponding number of metabolites (#) that changed over the 20-min incubation in each fraction (matrix, buffer).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-03-24 02:20:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/425958", "https://ndownloader.figshare.com/files/425966", "https://ndownloader.figshare.com/files/425985", "https://ndownloader.figshare.com/files/426000", "https://ndownloader.figshare.com/files/426022"], "description"=>"<div><h3>Background/Aim</h3><p>Incomplete or limited long-chain fatty acid (LCFA) combustion in skeletal muscle has been associated with insulin resistance. Signals that are responsive to shifts in LCFA β-oxidation rate or degree of intramitochondrial catabolism are hypothesized to regulate second messenger systems downstream of the insulin receptor. Recent evidence supports a causal link between mitochondrial LCFA combustion in skeletal muscle and insulin resistance. We have used unbiased metabolite profiling of mouse muscle mitochondria with the aim of identifying candidate metabolites within or effluxed from mitochondria and that are shifted with LCFA combustion rate.</p><h3>Methodology/Principal Findings</h3><p>Large-scale unbiased metabolomics analysis was performed using GC/TOF-MS on buffer and mitochondrial matrix fractions obtained prior to and after 20 min of palmitate catabolism (n = 7 mice/condition). Three palmitate concentrations (2, 9 and 19 µM; corresponding to low, intermediate and high oxidation rates) and 9 µM palmitate plus tricarboxylic acid (TCA) cycle and electron transport chain inhibitors were each tested and compared to zero palmitate control incubations. Paired comparisons of the 0 and 20 min samples were made by Student's t-test. False discovery rate were estimated and Type I error rates assigned. Major metabolite groups were organic acids, amines and amino acids, free fatty acids and sugar phosphates. Palmitate oxidation was associated with unique profiles of metabolites, a subset of which correlated to palmitate oxidation rate. In particular, palmitate oxidation rate was associated with distinct changes in the levels of TCA cycle intermediates within and effluxed from mitochondria.</p><h3>Conclusions/Significance</h3><p>This proof-of-principle study establishes that large-scale metabolomics methods can be applied to organelle-level models to discover metabolite patterns reflective of LCFA combustion, which may lead to identification of molecules linking muscle fat metabolism and insulin signaling. Our results suggest that future studies should focus on the fate of effluxed TCA cycle intermediates and on mechanisms ensuring their replenishment during LCFA metabolism in skeletal muscle.</p></div>", "links"=>[], "tags"=>["long-chain", "fatty", "combustion", "metabolite", "profiles", "skeletal", "mitochondria"], "article_id"=>144100, "categories"=>["Cancer", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0009834.s001", "https://dx.doi.org/10.1371/journal.pone.0009834.s002", "https://dx.doi.org/10.1371/journal.pone.0009834.s003", "https://dx.doi.org/10.1371/journal.pone.0009834.s004", "https://dx.doi.org/10.1371/journal.pone.0009834.s005"], "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Long_Chain_Fatty_Acid_Combustion_Rate_Is_Associated_with_Unique_Metabolite_Profiles_in_Skeletal_Muscle_Mitochondria/144100", "title"=>"Long-Chain Fatty Acid Combustion Rate Is Associated with Unique Metabolite Profiles in Skeletal Muscle Mitochondria", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-03-24 01:08:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/857142"], "description"=>"<p>Conditions: incubations with/without palmitate, in the absence or presence of inhibitors (inh; 10 mM malonate, 5 µM rotenone). Times: subsamples of mitochondrial suspension removed at 0 and 20 min for subsequent metabolomics determinations. Fractions: mitochondrial suspensions were separated into matrix (M) and buffer (B). GC/TOF-MS: gas chromatography, time-of-flight mass spectroscopy.</p>", "links"=>[], "tags"=>["metabolite", "shifts", "murine", "mitochondrial", "preparations", "rates", "lcfa"], "article_id"=>527562, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_experimental_design_used_to_determine_metabolite_shifts_in_murine_muscle_mitochondrial_preparations_under_different_rates_of_LCFA_946_oxidation_/527562", "title"=>"Summary of experimental design used to determine metabolite shifts in murine muscle mitochondrial preparations under different rates of LCFA β-oxidation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:06:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/857924"], "description"=>"<p>Significance: paired t-test, 0 <i>vs</i>. 20 min, within treatment; * P<0.05; **, P<0.02. See legend to <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009834#pone-0009834-g005\" target=\"_blank\">Figure 5</a> for further details.</p>", "links"=>[], "tags"=>["levels", "unidentified", "metabolites", "buffer", "matrix", "fractions", "mitochondrial"], "article_id"=>528364, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g008", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Change_over_time_in_levels_of_selected_unidentified_metabolites_in_buffer_and_matrix_fractions_obtained_from_muscle_mitochondrial_preparations_/528364", "title"=>"Change over time in levels of selected unidentified metabolites in buffer and matrix fractions obtained from muscle mitochondrial preparations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:19:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/857284"], "description"=>"<p>Metabolites are shown for which the concentration changed significantly during the 20-min incubation for one or more of the treatment conditions (0, 2, 9, and 19 µM palmitate, and 9 µM palmitate plus FAO inhibitors).</p>", "links"=>[], "tags"=>["metabolites", "murine", "mitochondrial", "preparations", "changed"], "article_id"=>527729, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g002", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_map_showing_the_identified_metabolites_from_murine_muscle_mitochondrial_preparations_that_changed_in_concentration_over_the_course_of_the_incubations_/527729", "title"=>"Heat map showing the identified metabolites from murine muscle mitochondrial preparations that changed in concentration over the course of the incubations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:08:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/857475"], "description"=>"<p>All 5 conditions are shown (0, 2, 9 and 19 µM palmitate, and 9 µM palmitate plus inhibitors). Values are the log of the change in concentration (peak height). Significance: paired t-test, 0 <i>vs</i>. 20 min, within treatment; * P<0.05; **, P<0.02, *** P<0.005.</p>", "links"=>[], "tags"=>["supplied", "substrates", "buffer", "murine", "mitochondria"], "article_id"=>527923, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Change_in_the_concentration_of_supplied_substrates_palmitate_malate_in_the_buffer_fraction_obtained_from_murine_muscle_mitochondria_over_the_course_of_the_incubations_/527923", "title"=>"Change in the concentration of supplied substrates (palmitate, malate) in the buffer fraction obtained from murine muscle mitochondria over the course of the incubations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:12:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/857396"], "description"=>"<p>Numbers of metabolites that changed significantly in concentration (P<0.05, paired t-test) in buffer and matrix fractions obtained from skeletal muscle mitochondria oxidizing LCFA at different rates.</p>", "links"=>[], "tags"=>["metabolites", "changed", "paired", "buffer", "matrix", "fractions", "skeletal", "mitochondria", "oxidizing", "lcfa"], "article_id"=>527828, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Numbers_of_metabolites_that_changed_significantly_in_concentration_P_lt_0_05_paired_t_test_in_buffer_and_matrix_fractions_obtained_from_skeletal_muscle_mitochondria_oxidizing_LCFA_at_different_rates_/527828", "title"=>"Numbers of metabolites that changed significantly in concentration (P<0.05, paired t-test) in buffer and matrix fractions obtained from skeletal muscle mitochondria oxidizing LCFA at different rates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:10:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/858055"], "description"=>"<p>Global characteristics of metabolomics dataset.</p>", "links"=>[], "tags"=>["characteristics", "metabolomics"], "article_id"=>528505, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.t001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_characteristics_of_metabolomics_dataset_/528505", "title"=>"Global characteristics of metabolomics dataset.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-03-24 02:21:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/857591"], "description"=>"<p>All 5 conditions are shown (0, 2, 9 and 19 µM palmitate, and 9 µM palmitate plus inhibitors) for both fractions (matrix and buffer). Values are the log of the change in concentration (peak height) over a 20-min incubation. Buffer and matrix fractions can be compared within each metabolite. Significance: paired t-test, 0 <i>vs</i>. 20 min, within treatment; * P<0.05; **, P<0.02, *** P<0.005. ‡: indicates that an outlier was removed from either the 0 or 20 min group for that metabolite in that fraction.</p>", "links"=>[], "tags"=>["tca", "intermediates", "buffer", "matrix", "fractions", "mitochondrial"], "article_id"=>528029, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_detected_TCA_cycle_intermediates_over_time_in_buffer_and_matrix_fractions_obtained_from_muscle_mitochondrial_preparations_/528029", "title"=>"Changes in detected TCA cycle intermediates over time in buffer and matrix fractions obtained from muscle mitochondrial preparations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:13:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/857758"], "description"=>"<p>Significance: paired t-test, 0 <i>vs</i>. 20 min, within treatment; * P<0.05; **, P<0.02, *** P<0.005. See legend to <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0009834#pone-0009834-g005\" target=\"_blank\">Figure 5</a> for further details.</p>", "links"=>[], "tags"=>["amino", "acids", "buffer", "matrix", "fractions", "mitochondrial"], "article_id"=>528190, "categories"=>["Virology", "Biochemistry", "Neuroscience"], "users"=>["Erin L. Seifert", "Oliver Fiehn", "Véronic Bezaire", "David R. Bickel", "Gert Wohlgemuth", "Sean H. Adams", "Mary-Ellen Harper"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0009834.g006", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_detected_amino_acids_over_time_in_buffer_and_matrix_fractions_obtained_from_muscle_mitochondrial_preparations_/528190", "title"=>"Changes in detected amino acids over time in buffer and matrix fractions obtained from muscle mitochondrial preparations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-03-24 02:16:30"}

PMC Usage Stats | Further Information

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

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