Intestinal Microbial Ecology and Environmental Factors Affecting Necrotizing Enterocolitis
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{"title"=>"Intestinal microbial ecology and environmental factors affecting necrotizing enterocolitis", "type"=>"journal", "authors"=>[{"first_name"=>"Roberto Murgas", "last_name"=>"Torrazza", "scopus_author_id"=>"36651673400"}, {"first_name"=>"Maria", "last_name"=>"Ukhanova", "scopus_author_id"=>"54889354800"}, {"first_name"=>"Xiaoyu", "last_name"=>"Wang", "scopus_author_id"=>"54682531200"}, {"first_name"=>"Renu", "last_name"=>"Sharma", "scopus_author_id"=>"55685396500"}, {"first_name"=>"Mark Lawrence", "last_name"=>"Hudak", "scopus_author_id"=>"7004585564"}, {"first_name"=>"Josef", "last_name"=>"Neu", "scopus_author_id"=>"7006433651"}, {"first_name"=>"Volker", "last_name"=>"Mai", "scopus_author_id"=>"7006952659"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0083304", "scopus"=>"2-s2.0-84893560224", "sgr"=>"84893560224", "pmid"=>"24386174", "issn"=>"19326203", "pui"=>"372325129", "isbn"=>"1932-6203"}, "id"=>"6a250273-e338-3245-8b18-c2b924382dc8", "abstract"=>"Necrotizing enterocolitis (NEC) is the most devastating intestinal disease affecting preterm infants. In addition to being associated with short term mortality and morbidity, survivors are left with significant long term sequelae. The cost of caring for these infants is high. Epidemiologic evidence suggests that use of antibiotics and type of feeding may cause an intestinal dysbiosis important in the pathogenesis of NEC, but the contribution of specific infectious agents is poorly understood. Fecal samples from preterm infants ≤32 weeks gestation were analyzed using 16S rRNA based methods at 2, 1, and 0 weeks, prior to diagnosis of NEC in 18 NEC cases and 35 controls. Environmental factors such as antibiotic usage, feeding type (human milk versus formula) and location of neonatal intensive care unit (NICU) were also evaluated. Microbiota composition differed between the three neonatal units where we observed differences in antibiotic usage. In NEC cases we observed a higher proportion of Proteobacteria (61%) two weeks and of Actinobacteria (3%) 1 week before diagnosis of NEC compared to controls (19% and 0.4%, respectively) and lower numbers of Bifidobacteria counts and Bacteroidetes proportions in the weeks before NEC diagnosis. In the first fecal samples obtained during week one of life we detected a novel signature sequence, distinct from but matching closest to Klebsiella pneumoniae, that was strongly associated with NEC development later in life. Infants who develop NEC exhibit a different pattern of microbial colonization compared to controls. Antibiotic usage correlated with these differences and combined with type of feeding likely plays a critical role in the development of NEC.", "link"=>"http://www.mendeley.com/research/intestinal-microbial-ecology-environmental-factors-affecting-necrotizing-enterocolitis-1", "reader_count"=>75, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>16, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>7, "Other"=>3, "Student > Master"=>14, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>16, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>7, "Other"=>3, "Student > Master"=>14, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Medicine and Dentistry"=>38, "Agricultural and Biological Sciences"=>18, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>38}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1, "United Kingdom"=>2, "Spain"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1332043"], "description"=>"<p>Baseline Characteristics of the Infants. (Mean ± SD).</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology"], "article_id"=>889022, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Baseline_Characteristics_of_the_Infants_Mean_177_SD_/889022", "title"=>"Baseline Characteristics of the Infants. (Mean ± SD).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332039"], "description"=>"<p>* p-value 2 weeks before NEC <0.05; **p-value week of NEC <0.05.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "fecal", "counts"], "article_id"=>889018, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g007", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qPCR_for_fecal_counts_of_Bifidobacteria_/889018", "title"=>"qPCR for fecal counts of Bifidobacteria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332033"], "description"=>"<p>Proportions of the major bacterial phyla at A) two weeks before, B) one week before, and C) during week of NEC diagnosis for individual samples from controls (c_###) and NEC cases (n_###) and means for samples combined by NEC status (control, NEC).</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "proportions", "bacterial"], "article_id"=>889012, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_proportions_of_bacterial_phyla_/889012", "title"=>"Changes in proportions of bacterial phyla.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332030"], "description"=>"<p>Principal component analysis (PCA) of overall diversity based on UniFrac (unweighted) metric A) 2 weeks before; B) 1 week before; and C) week of diagnosis of NEC. Squares represent controls and triangles represent cases. P1 is component 1 and P2 component 2.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology"], "article_id"=>889009, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unifrac_diversity_measures_/889009", "title"=>"Unifrac diversity measures.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332028"], "description"=>"<p>Chao diversity was calculated from the OTU distribution A) 2 weeks before diagnosis of NEC; B) 1 week before diagnosis of NEC; and C) Week of diagnosis of NEC. As a measure of beta (within sample) diversity it is an estimate of the expected total number of OTUs detected in the sample if sequenced to completion.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "rarefaction"], "article_id"=>889007, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chao_rarefaction_diversity_/889007", "title"=>"Chao rarefaction diversity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332042"], "description"=>"<p>Antibiotic exposure before NEC # prescribed antibiotic/# in group (%).</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "nec", "prescribed"], "article_id"=>889021, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.t003", "stats"=>{"downloads"=>3, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antibiotic_exposure_before_NEC_prescribed_antibiotic_in_group_/889021", "title"=>"Antibiotic exposure before NEC # prescribed antibiotic/# in group (%).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332027"], "description"=>"<p>Each row represents a separate OTU with the closest match in the database listed on the right. Each column represents an individual sample from both cases and controls at each of the three time points. OTUs are listed in order of dominance with the most dominant on the top. Darker color indicates higher number of sequences in this OTU in an individual sample (see color code in left corner). Darkest shade indicates 50+ sequence reads obtain for that OTU in that sample.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology"], "article_id"=>889006, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dominant_OTU_s_/889006", "title"=>"Dominant OTU's.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332041"], "description"=>"<p>Major Clinical Outcomes. # cases/# in group (%).</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology"], "article_id"=>889020, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Major_Clinical_Outcomes_cases_in_group_/889020", "title"=>"Major Clinical Outcomes. # cases/# in group (%).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332038"], "description"=>"<p>Controls are shown on the left (c_###) and NEC cases on the right (n_###). The number of sequences detected per sample for each OTU is indicated by degree of shading, with the darkest shade correlating with the highest number of sequences. OTUs more frequently observed in NEC cases are shown on the top and OTUs less frequently observed are shown on the bottom.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "otu", "correlating", "nec"], "article_id"=>889017, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g006", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_map_of_selected_OTU_98_similarity_correlating_with_NEC_status_during_the_week_of_diagnosis_/889017", "title"=>"Heat map of selected OTU (98% similarity) correlating with NEC status during the week of diagnosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332035"], "description"=>"<p>Differences in the proportions of prevalent bacterial phyla, based on 454 16S rRNA sequencing, in controls at week 0 in A) Jacksonville and B) Gainesville.</p>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "proportions", "prevalent", "bacterial", "454", "16s", "rrna", "controls", "jacksonville"], "article_id"=>889014, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083304.g005", "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_the_proportions_of_prevalent_bacterial_phyla_based_on_454_16S_rRNA_sequencing_in_controls_at_week_0_in_A_Jacksonville_and_B_Gainesville_/889014", "title"=>"Differences in the proportions of prevalent bacterial phyla, based on 454 16S rRNA sequencing, in controls at week 0 in A) Jacksonville and B) Gainesville.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-30 03:09:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1332046", "https://ndownloader.figshare.com/files/1332047", "https://ndownloader.figshare.com/files/1332048"], "description"=>"<div><p>Necrotizing enterocolitis (NEC) is the most devastating intestinal disease affecting preterm infants. In addition to being associated with short term mortality and morbidity, survivors are left with significant long term sequelae. The cost of caring for these infants is high. Epidemiologic evidence suggests that use of antibiotics and type of feeding may cause an intestinal dysbiosis important in the pathogenesis of NEC, but the contribution of specific infectious agents is poorly understood. Fecal samples from preterm infants ≤32 weeks gestation were analyzed using 16S rRNA based methods at 2, 1, and 0 weeks, prior to diagnosis of NEC in 18 NEC cases and 35 controls. Environmental factors such as antibiotic usage, feeding type (human milk versus formula) and location of neonatal intensive care unit (NICU) were also evaluated. Microbiota composition differed between the three neonatal units where we observed differences in antibiotic usage. In NEC cases we observed a higher proportion of Proteobacteria (61%) two weeks and of Actinobacteria (3%) 1 week before diagnosis of NEC compared to controls (19% and 0.4%, respectively) and lower numbers of Bifidobacteria counts and Bacteroidetes proportions in the weeks before NEC diagnosis. In the first fecal samples obtained during week one of life we detected a novel signature sequence, distinct from but matching closest to <i>Klebsiella pneumoniae</i>, that was strongly associated with NEC development later in life. Infants who develop NEC exhibit a different pattern of microbial colonization compared to controls. Antibiotic usage correlated with these differences and combined with type of feeding likely plays a critical role in the development of NEC.</p></div>", "links"=>[], "tags"=>["microbiology", "Medical microbiology", "Complementary and alternative medicine", "epidemiology", "Pediatric epidemiology", "Gastroenterology and hepatology", "Pediatric gastroenterology", "Infectious diseases", "Gastrointestinal infections", "nutrition", "pediatrics", "Neonatology", "microbial", "ecology", "affecting", "necrotizing"], "article_id"=>889025, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Roberto Murgas Torrazza", "Maria Ukhanova", "Xiaoyu Wang", "Renu Sharma", "Mark Lawrence Hudak", "Josef Neu", "Volker Mai"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083304.s001", "https://dx.doi.org/10.1371/journal.pone.0083304.s002", "https://dx.doi.org/10.1371/journal.pone.0083304.s003"], "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intestinal_Microbial_Ecology_and_Environmental_Factors_Affecting_Necrotizing_Enterocolitis_/889025", "title"=>"Intestinal Microbial Ecology and Environmental Factors Affecting Necrotizing Enterocolitis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-12-30 03:09:18"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"22", "full-text"=>"23", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
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  • {"unique-ip"=>"108", "full-text"=>"130", "pdf"=>"71", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"43", "full-text"=>"47", "pdf"=>"53", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"40", "full-text"=>"47", "pdf"=>"28", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"16", "full-text"=>"21", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"19", "full-text"=>"23", "pdf"=>"15", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"16", "full-text"=>"23", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"18", "full-text"=>"13", "pdf"=>"13", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Anatomy", "average_usage"=>[248, 440, 562, 666, 765, 856, 944, 1028, 1112, 1198, 1282, 1362, 1430]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Medicine and health sciences/Anatomy", "average_usage"=>[248, 441, 564, 668, 769, 859, 948, 1034, 1117, 1202, 1290, 1368, 1437]}, {"subject_area"=>"/Medicine and health sciences/Physiology", "average_usage"=>[258, 449, 572, 679, 775, 866, 956, 1041, 1124, 1211, 1291, 1371, 1437]}, {"subject_area"=>"/People and places/Population groupings", "average_usage"=>[265, 456, 578, 682, 782, 881, 965, 1053, 1133, 1223, 1310, 1391, 1457]}]}
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