Impact of Amino Acid Substitutions in B Subunit of DNA Gyrase in Mycobacterium leprae on Fluoroquinolone Resistance
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{"title"=>"Impact of Amino Acid Substitutions in B Subunit of DNA Gyrase in Mycobacterium leprae on Fluoroquinolone Resistance", "type"=>"journal", "authors"=>[{"first_name"=>"Kazumasa", "last_name"=>"Yokoyama", "scopus_author_id"=>"55740408600"}, {"first_name"=>"Hyun", "last_name"=>"Kim", "scopus_author_id"=>"55775278200"}, {"first_name"=>"Tetsu", "last_name"=>"Mukai", "scopus_author_id"=>"7401555653"}, {"first_name"=>"Masanori", "last_name"=>"Matsuoka", "scopus_author_id"=>"7401543171"}, {"first_name"=>"Chie", "last_name"=>"Nakajima", "scopus_author_id"=>"9746068400"}, {"first_name"=>"Yasuhiko", "last_name"=>"Suzuki", "scopus_author_id"=>"8964195600"}], "year"=>2012, "source"=>"PLoS Neglected Tropical Diseases", "identifiers"=>{"scopus"=>"2-s2.0-84869048076", "pui"=>"366040826", "doi"=>"10.1371/journal.pntd.0001838", "issn"=>"19352727", "pmid"=>"23071850", "sgr"=>"84869048076"}, "id"=>"ac0c72d4-fe3b-3757-92b1-4a282adcae51", "abstract"=>"BACKGROUND: Ofloxacin is a fluoroquinolone (FQ) used for the treatment of leprosy. FQs are known to interact with both A and B subunits of DNA gyrase and inhibit supercoiling activity of this enzyme. Mutations conferring FQ resistance have been reported to be found only in the gene encoding A subunit of this enzyme (gyrA) of M. leprae, although there are many reports on the FQ resistance-associated mutation in gyrB in other bacteria, including M. tuberculosis, a bacterial species in the same genus as M. leprae.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: To reveal the possible contribution of mutations in gyrB to FQ resistance in M. leprae, we examined the inhibitory activity of FQs against recombinant DNA gyrases with amino acid substitutions at position 464, 502 and 504, equivalent to position 461, 499 and 501 in M. tuberculosis, which are reported to contribute to reduced sensitivity to FQ. The FQ-inhibited supercoiling assay and FQ-induced cleavage assay demonstrated the important roles of these amino acid substitutions in reduced sensitivity to FQ with marked influence by amino acid substitution, especially at position 502. Additionally, effectiveness of sitafloxacin, a FQ, to mutant DNA gyrases was revealed by low inhibitory concentration of this FQ.\\n\\nSIGNIFICANCE: Data obtained in this study suggested the possible emergence of FQ-resistant M. leprae with mutations in gyrB and the necessity of analyzing both gyrA and gyrB for an FQ susceptibility test. In addition, potential use of sitafloxacin for the treatment of problematic cases of leprosy by FQ resistant M. leprae was suggested.", "link"=>"http://www.mendeley.com/research/impact-amino-acid-substitutions-b-subunit-dna-gyrase-mycobacterium-leprae-fluoroquinolone-resistance-2", "reader_count"=>17, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>2, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Materials Science"=>1, "Agricultural and Biological Sciences"=>8, "Medicine and Dentistry"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Brazil"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/559524"], "description"=>"<p>IC<sub>50</sub>s and CC<sub>25</sub>s were calculated by the quinolone-inhibited supercoiling assay and FQ-mediated cleavage assay, respectively. Fold increase of each FQ for mutant DNA gyrases was plotted. (A) IC<sub>50</sub>s, (B) CC<sub>25</sub>s. Open, closed and hatched bar denotes the value for GyrB- GyrB-Asp464Asn, GyrB-Asn502Asp and GyrB-Glu504Val DNA gyrase, respectively.</p>", "links"=>[], "tags"=>["fqs", "mutant", "dna"], "article_id"=>230016, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.g005", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_IC_50_s_and_CC_25_s_of_FQs_for_mutant_DNA_gyrases_/230016", "title"=>"Increased IC<sub>50</sub>s and CC<sub>25</sub>s of FQs for mutant DNA gyrases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-11 00:00:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/559648"], "description"=>"<p>IC<sub>50</sub>s and CC<sub>25</sub>s of FQs against WT and mutant DNA gyrases.</p>", "links"=>[], "tags"=>["fqs", "wt", "mutant", "dna"], "article_id"=>230144, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.t002", "stats"=>{"downloads"=>5, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IC_50_s_and_CC_25_s_of_FQs_against_WT_and_mutant_DNA_gyrases_/230144", "title"=>"IC<sub>50</sub>s and CC<sub>25</sub>s of FQs against WT and mutant DNA gyrases.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-11 00:02:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/298140", "https://ndownloader.figshare.com/files/298155", "https://ndownloader.figshare.com/files/298179", "https://ndownloader.figshare.com/files/298211"], "description"=>"<div><h3>Background</h3><p>Ofloxacin is a fluoroquinolone (FQ) used for the treatment of leprosy. FQs are known to interact with both A and B subunits of DNA gyrase and inhibit supercoiling activity of this enzyme. Mutations conferring FQ resistance have been reported to be found only in the gene encoding A subunit of this enzyme (<em>gyrA</em>) of <em>M. leprae</em>, although there are many reports on the FQ resistance-associated mutation in <em>gyrB</em> in other bacteria, including <em>M. tuberculosis</em>, a bacterial species in the same genus as <em>M. leprae</em>.</p> <h3>Methodology/Principal Findings</h3><p>To reveal the possible contribution of mutations in <em>gyrB</em> to FQ resistance in <em>M. leprae</em>, we examined the inhibitory activity of FQs against recombinant DNA gyrases with amino acid substitutions at position 464, 502 and 504, equivalent to position 461, 499 and 501 in <em>M. tuberculosis</em>, which are reported to contribute to reduced sensitivity to FQ. The FQ-inhibited supercoiling assay and FQ-induced cleavage assay demonstrated the important roles of these amino acid substitutions in reduced sensitivity to FQ with marked influence by amino acid substitution, especially at position 502. Additionally, effectiveness of sitafloxacin, a FQ, to mutant DNA gyrases was revealed by low inhibitory concentration of this FQ.</p> <h3>Significance</h3><p>Data obtained in this study suggested the possible emergence of FQ-resistant <em>M. leprae</em> with mutations in <em>gyrB</em> and the necessity of analyzing both <em>gyrA</em> and <em>gyrB</em> for an FQ susceptibility test. In addition, potential use of sitafloxacin for the treatment of problematic cases of leprosy by FQ resistant <em>M. leprae</em> was suggested.</p> </div>", "links"=>[], "tags"=>["amino", "substitutions", "subunit", "dna", "gyrase", "fluoroquinolone"], "article_id"=>118788, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001838.s001", "https://dx.doi.org/10.1371/journal.pntd.0001838.s002", "https://dx.doi.org/10.1371/journal.pntd.0001838.s003", "https://dx.doi.org/10.1371/journal.pntd.0001838.s004"], "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Impact_of_Amino_Acid_Substitutions_in_B_Subunit_of_DNA_Gyrase_in_Mycobacterium_leprae_on_Fluoroquinolone_Resistance/118788", "title"=>"Impact of Amino Acid Substitutions in B Subunit of DNA Gyrase in <em>Mycobacterium leprae</em> on Fluoroquinolone Resistance", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-10-11 02:26:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/559001"], "description"=>"<p>(A) amino acid number of GyrB in <i>E. coli</i>, (B) Amino acid number, nucleotide sequences and amino acid sequence of WT <i>M. leprae</i> GyrB QRDR, (C) Amino acid number, nucleotide sequences and of WT <i>M. tuberculosis</i> GyrB QRDR, (D) Altered amino acids and corresponding nucleotide substitutions found in higher rate in FQ-resistant <i>M. tuberculosis</i> isolates.</p>", "links"=>[], "tags"=>["amino", "sequences", "qrdr", "tuberculosis", "mutations", "fq-resistant"], "article_id"=>229486, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.g001", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nucleotide_and_amino_acid_sequences_of_QRDR_of_M_leprae_and_M_tuberculosis_gyrB_and_mutations_found_in_FQ_resistant_isolates_/229486", "title"=>"Nucleotide and amino acid sequences of QRDR of <i>M. leprae</i> and <i>M. tuberculosis gyrB</i> and mutations found in FQ-resistant isolates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-11 02:38:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/559154"], "description"=>"<p>(A) Primer pairs k-54+D464N_Rv, N502D_Rvor E504V_Rv (<a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001838#pntd-0001838-t001\" target=\"_blank\">Table 1</a>) were used for amplifying the DNA fragment encoding N-terminus half (amino acid 424 to 467, 505 or 507, respectively) of C-terminus region of GyrB carrying Asp464Asn, Asn502Asp and Glu504Val, respectively. Primer pairs k-55+D464N_Fw, N502D_Fw or E504V_Fw (<a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001838#pntd-0001838-t001\" target=\"_blank\">Table 1</a>) were used for amplifying the DNA fragment encoding the C-terminus half (amino acid 461, 499 or 501 to 678, respectively) of the C-terminus region of GyrB carrying Asp464Asn, Asn502Asp and Glu504Val, respectively. (B) To complete the C-terminus region encoding cassette, DNA fragments encoding the N-terminus half and C-terminus half of the C-terminus region of GyrB were annealed and reamplified by PCR using the primer pair of k-54 and k-55. (C) The mutated <i>gyrB</i>-C cassettes were digested with <i>Pml</i>I and <i>Xho</i>I restriction endonucleases and ligated into the expression plasmid containing the WT<i>gyrB</i>N-terminus region DNA fragment digested by the same enzymes.</p>", "links"=>[], "tags"=>["wt", "mutant", "dna", "gyrase"], "article_id"=>229648, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Construction_of_WT_and_mutant_DNA_gyrase_expression_plasmid_/229648", "title"=>"Construction of WT and mutant DNA gyrase expression plasmid.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-11 02:40:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/559313"], "description"=>"<p>Relaxed pBR322 (0.3 mg) was incubated with GyrA (50 ng) and GyrB (50 ng) in the presence of the indicated concentration of OFX. FQ-inhibited supercoiling activity assay was performed in combination of WTGyrA+WTGyrB (A), GyrB-Asp464Asn (B), GyrB-Asn502Asp (C) and GyrB-Glu504Val (D). R and SC denote relaxed and supercoiled pBR322 DNA, respectively.</p>", "links"=>[], "tags"=>["dna", "supercoiling"], "article_id"=>229810, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_OFX_inhibited_DNA_supercoiling_assay_/229810", "title"=>"OFX-inhibited DNA supercoiling assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-11 02:43:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/559607"], "description"=>"<p>Mutated codons are indicated in bold face.</p>", "links"=>[], "tags"=>["sequences", "primers"], "article_id"=>230101, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.t001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nucleotide_sequences_of_primers_used_in_this_study_/230101", "title"=>"Nucleotide sequences of primers used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-11 00:01:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/559416"], "description"=>"<p>Supercoiled pBR322 (0.3 mg) was incubated with GyrA (50 ng) and GyrB (50 ng) in the presence of the indicated concentration of OFX. DNA cleavage assay was performed in combination of WT GyrA+WT GyrB (A), GyrB-Asp464Asn (B), GyrB-Asn502Asp (C) and GyrB-Glu504Val (D). R, L and SC denote relaxed, linear and supercoiled pBR322 DNA, respectively.</p>", "links"=>[], "tags"=>["dna", "cleavage"], "article_id"=>229914, "categories"=>["Microbiology"], "users"=>["Kazumasa Yokoyama", "Hyun Kim", "Tetsu Mukai", "Masanori Matsuoka", "Chie Nakajima", "Yasuhiko Suzuki"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0001838.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_OFX_mediated_DNA_cleavage_assay_/229914", "title"=>"OFX-mediated DNA cleavage assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-11 02:45:14"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"35", "full-text"=>"39", "pdf"=>"29", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"10"}
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  • {"unique-ip"=>"24", "full-text"=>"28", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"2"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"4"}
  • {"unique-ip"=>"33", "full-text"=>"31", "pdf"=>"22", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"11"}
  • {"unique-ip"=>"16", "full-text"=>"17", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2013", "month"=>"5"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2013", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2013", "month"=>"8"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"12"}
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  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"6", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"6"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
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  • {"unique-ip"=>"11", "full-text"=>"4", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "abstract"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2014", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
  • {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "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"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"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"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"5", "full-text"=>"3", "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"=>"10", "full-text"=>"4", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"2", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"4", "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"=>"5", "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"=>"1"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"unique-ip"=>"3", "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"=>"8"}
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  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
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  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"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"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"8", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "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", "average_usage"=>[322, 550, 671, 773, 864, 955, 1048, 1135, 1223, 1308, 1387, 1465, 1534, 1602, 1673, 1744, 1813, 1885, 1955, 2026, 2093, 2160, 2228, 2290, 2349]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[324, 551, 679, 782, 879, 971, 1064, 1154, 1245, 1328, 1406, 1476, 1541, 1617, 1683, 1754, 1818, 1893, 1962, 2025, 2092, 2164, 2227, 2294, 2355]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[331, 557, 677, 777, 868, 960, 1050, 1136, 1223, 1307, 1390, 1466, 1536, 1603, 1673, 1741, 1814, 1889, 1954, 2028, 2096, 2164, 2233, 2305, 2362]}, {"subject_area"=>"/Medicine and health sciences/Tropical diseases", "average_usage"=>[318, 641, 793, 914, 1020, 1113, 1234, 1345, 1446, 1565, 1664, 1752, 1824, 1900, 1980, 2054, 2132, 2215, 2270, 2358, 2434, 2498, 2579, 2629, 2698]}, {"subject_area"=>"/Physical sciences", "average_usage"=>[304, 506, 616, 712, 799, 879, 968, 1052, 1134, 1212, 1284, 1357, 1427, 1494, 1557, 1621, 1689, 1756, 1823, 1883, 1944, 1997, 2056, 2118, 2171]}, {"subject_area"=>"/Physical sciences/Chemistry", "average_usage"=>[302, 508, 622, 720, 804, 888, 973, 1054, 1141, 1219, 1299, 1370, 1442, 1511, 1574, 1644, 1711, 1782, 1846, 1911, 1971, 2030, 2097, 2155, 2217]}]}
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