Extensive Genetic Diversity, Unique Population Structure and Evidence of Genetic Exchange in the Sexually Transmitted Parasite Trichomonas vaginalis
Publication Date
March 27, 2012
Journal
PLOS Neglected Tropical Diseases
Authors
Melissa D. Conrad, Andrew W. Gorman, Julia A. Schillinger, Pier Luigi Fiori, et al
Volume
6
Issue
3
Pages
e1573
DOI
http://doi.org/10.1371/journal.pntd.0001573
Publisher URL
http://journals.plos.org/plosntds/article?id=10.1371%2Fjournal.pntd.0001573
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22479659
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3313929
Europe PMC
http://europepmc.org/abstract/MED/22479659
Web of Science
000302132100025
Scopus
84859193494
Mendeley
http://www.mendeley.com/research/extensive-genetic-diversity-unique-population-structure-evidence-genetic-exchange-sexually-transmitt
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Mendeley | Further Information

{"title"=>"Extensive genetic diversity, unique population structure and evidence of genetic exchange in the sexually transmitted parasite Trichomonas vaginalis", "type"=>"journal", "authors"=>[{"first_name"=>"Melissa D.", "last_name"=>"Conrad", "scopus_author_id"=>"55157855900"}, {"first_name"=>"Andrew W.", "last_name"=>"Gorman", "scopus_author_id"=>"55157088400"}, {"first_name"=>"Julia A.", "last_name"=>"Schillinger", "scopus_author_id"=>"7003321388"}, {"first_name"=>"Pier Luigi", "last_name"=>"Fiori", "scopus_author_id"=>"7006216344"}, {"first_name"=>"Rossana", "last_name"=>"Arroyo", "scopus_author_id"=>"56013688300"}, {"first_name"=>"Nancy", "last_name"=>"Malla", "scopus_author_id"=>"7004159191"}, {"first_name"=>"Mohan Lal", "last_name"=>"Dubey", "scopus_author_id"=>"7004346361"}, {"first_name"=>"Jorge", "last_name"=>"Gonzalez", "scopus_author_id"=>"7404494177"}, {"first_name"=>"Susan", "last_name"=>"Blank", "scopus_author_id"=>"7004460439"}, {"first_name"=>"William E.", "last_name"=>"Secor", "scopus_author_id"=>"7004063907"}, {"first_name"=>"Jane M.", "last_name"=>"Carlton", "scopus_author_id"=>"26643079100"}], "year"=>2012, "source"=>"PLoS Neglected Tropical Diseases", "identifiers"=>{"sgr"=>"84859193494", "scopus"=>"2-s2.0-84859193494", "doi"=>"10.1371/journal.pntd.0001573", "isbn"=>"1935-2735 (Electronic)\\r1935-2727 (Linking)", "pui"=>"364547183", "issn"=>"19352727", "pmid"=>"22479659"}, "id"=>"a6060ada-5cb1-3e35-980e-b187d1527be0", "abstract"=>"BACKGROUND: Trichomonas vaginalis is the causative agent of human trichomoniasis, the most common non-viral sexually transmitted infection world-wide. Despite its prevalence, little is known about the genetic diversity and population structure of this haploid parasite due to the lack of appropriate tools. The development of a panel of microsatellite makers and SNPs from mining the parasite's genome sequence has paved the way to a global analysis of the genetic structure of the pathogen and association with clinical phenotypes.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Here we utilize a panel of T. vaginalis-specific genetic markers to genotype 235 isolates from Mexico, Chile, India, Australia, Papua New Guinea, Italy, Africa and the United States, including 19 clinical isolates recently collected from 270 women attending New York City sexually transmitted disease clinics. Using population genetic analysis, we show that T. vaginalis is a genetically diverse parasite with a unique population structure consisting of two types present in equal proportions world-wide. Parasites belonging to the two types (type 1 and type 2) differ significantly in the rate at which they harbor the T. vaginalis virus, a dsRNA virus implicated in parasite pathogenesis, and in their sensitivity to the widely-used drug, metronidazole. We also uncover evidence of genetic exchange, indicating a sexual life-cycle of the parasite despite an absence of morphologically-distinct sexual stages.\\n\\nCONCLUSIONS/SIGNIFICANCE: Our study represents the first robust and comprehensive evaluation of global T. vaginalis genetic diversity and population structure. Our identification of a unique two-type structure, and the clinically relevant phenotypes associated with them, provides a new dimension for understanding T. vaginalis pathogenesis. In addition, our demonstration of the possibility of genetic exchange in the parasite has important implications for genetic research and control of the disease.", "link"=>"http://www.mendeley.com/research/extensive-genetic-diversity-unique-population-structure-evidence-genetic-exchange-sexually-transmitt", "reader_count"=>49, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>9, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>4, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>9, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Medicine and Dentistry"=>9, "Agricultural and Biological Sciences"=>27, "Business, Management and Accounting"=>1, "Chemistry"=>2, "Immunology and Microbiology"=>5, "Nursing and Health Professions"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "Taiwan"=>1, "Brazil"=>1, "Spain"=>1}, "group_count"=>0}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/339621", "https://ndownloader.figshare.com/files/339680", "https://ndownloader.figshare.com/files/339735", "https://ndownloader.figshare.com/files/339818", "https://ndownloader.figshare.com/files/339867", "https://ndownloader.figshare.com/files/339964", "https://ndownloader.figshare.com/files/339984", "https://ndownloader.figshare.com/files/340035", "https://ndownloader.figshare.com/files/340083"], "description"=>"<div><h3>Background</h3><p><em>Trichomonas vaginalis</em> is the causative agent of human trichomoniasis, the most common non-viral sexually transmitted infection world-wide. Despite its prevalence, little is known about the genetic diversity and population structure of this haploid parasite due to the lack of appropriate tools. The development of a panel of microsatellite makers and SNPs from mining the parasite's genome sequence has paved the way to a global analysis of the genetic structure of the pathogen and association with clinical phenotypes.</p> <h3>Methodology/Principal Findings</h3><p>Here we utilize a panel of <em>T. vaginalis</em>-specific genetic markers to genotype 235 isolates from Mexico, Chile, India, Australia, Papua New Guinea, Italy, Africa and the United States, including 19 clinical isolates recently collected from 270 women attending New York City sexually transmitted disease clinics. Using population genetic analysis, we show that <em>T. vaginalis</em> is a genetically diverse parasite with a unique population structure consisting of two types present in equal proportions world-wide. Parasites belonging to the two types (type 1 and type 2) differ significantly in the rate at which they harbor the <em>T. vaginalis</em> virus, a dsRNA virus implicated in parasite pathogenesis, and in their sensitivity to the widely-used drug, metronidazole. We also uncover evidence of genetic exchange, indicating a sexual life-cycle of the parasite despite an absence of morphologically-distinct sexual stages.</p> <h3>Conclusions/Significance</h3><p>Our study represents the first robust and comprehensive evaluation of global <em>T. vaginalis</em> genetic diversity and population structure. Our identification of a unique two-type structure, and the clinically relevant phenotypes associated with them, provides a new dimension for understanding <em>T. vaginalis</em> pathogenesis. In addition, our demonstration of the possibility of genetic exchange in the parasite has important implications for genetic research and control of the disease.</p> </div>", "links"=>[], "tags"=>["transmitted", "parasite"], "article_id"=>127147, "categories"=>["Cancer", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.s001", "https://dx.doi.org/10.1371/journal.pntd.0001573.s002", "https://dx.doi.org/10.1371/journal.pntd.0001573.s003", "https://dx.doi.org/10.1371/journal.pntd.0001573.s004", "https://dx.doi.org/10.1371/journal.pntd.0001573.s005", "https://dx.doi.org/10.1371/journal.pntd.0001573.s006", "https://dx.doi.org/10.1371/journal.pntd.0001573.s007", "https://dx.doi.org/10.1371/journal.pntd.0001573.s008", "https://dx.doi.org/10.1371/journal.pntd.0001573.s009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Extensive_Genetic_Diversity_Unique_Population_Structure_and_Evidence_of_Genetic_Exchange_in_the_Sexually_Transmitted_Parasite_Trichomonas_vaginalis_/127147", "title"=>"Extensive Genetic Diversity, Unique Population Structure and Evidence of Genetic Exchange in the Sexually Transmitted Parasite <em>Trichomonas vaginalis</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-03-27 01:59:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/662464"], "description"=>"<p>A Bayesian clustering model implemented in STRUCTURE 2.2 indicates a two-cluster population structure for <i>T. vaginalis</i> (N = 188). The green cluster (type 1, (N = 95)) and red cluster (type 2, (N = 93) are found in each geographical location, with the exception of Southern Africa where all samples are type 1, and Mexico, which has a statistically significant over-representation of type 2. PNG: Papua New Guinea. Isolates included in each geographical location can be found in <b><a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001573#pntd.0001573.s006\" target=\"_blank\">Table S1</a></b>.</p>", "links"=>[], "tags"=>["Infectious diseases", "Evolutionary biology"], "article_id"=>332943, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_cluster_population_structure_of_T_vaginalis_/332943", "title"=>"Two cluster population structure of <i>T. vaginalis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-27 00:49:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/662557"], "description"=>"<p>(<b>A</b>) Phylogenetic tree of the evolutionary relationship of type 1 (green, N = 37) and type 2 (red, N = 57) single copy gene protein sequences, with <i>Pentatrichomonas hominis</i> and <i>Tritrichomonas foetus</i> protein sequences as outgroups. Protein sequences for CRN, PMS1 and Mlh1a were concatenated for each isolate and the tree was bootstrapped 1000 times. BioNJ methods were used for tree reconstruction. Blue dots indicate nodes where bootstrap support is ≥50. (<b>B</b>) The allelic richness by type was calculated with ADZE using microsatellite data for all isolates. Type 1 (green, N = 76) shows greater allelic richness than type 2 (red, N = 64), supporting the former as the ancestral clade and the latter as derived.</p>", "links"=>[], "tags"=>["1-like", "parasites"], "article_id"=>333037, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Type_1_like_parasites_appear_to_have_given_rise_to_type_2_parasites_/333037", "title"=>"Type 1-like parasites appear to have given rise to type 2 parasites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-27 00:50:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/662659"], "description"=>"<p>(A) Pairwise linkage disequilibrium (LD) matrix for MS genotypes of type 1 (N = 95) and 2 (N = 93). Significant LD is highlighted in red. Type 2, with 42 cases of paired locus LD, shows a greater amount of LD in comparison to type 1 with 15 cases. (B) Heat maps indicating degree of LD between SNPs in single copy genes. Gene boundaries are indicated by black lines. The number of pairwise comparisons varies between the two types due to the difference in the number of polymorphisms analyzed, but a greater amount of pairwise LD in type 2 in comparison to type 1 is indicated.</p>", "links"=>[], "tags"=>["disequilibrium", "varies"], "article_id"=>333140, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Linkage_disequilibrium_varies_between_type_/333140", "title"=>"Linkage disequilibrium varies between type.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-27 00:52:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/662766"], "description"=>"<p>Phylogenetic trees were inferred from the DNA sequences for each of the three single copy genes (A) CRN (N = 94), (B) PMS1 (N = 94), and (C) Mlh1a (N = 94), and from the concatenation of all the three genes (N = 94; D). Blue dots indicate nodes where bootstrap support is ≥50. The clustering of type 1 (green) and type 2 (red) isolates supports the two-type population structure. Instances of unlike clustering resulting in non-homologous tree topology provide possible evidence for cases of recombination.</p>", "links"=>[], "tags"=>["single-copy"], "article_id"=>333246, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenies_of_single_copy_genes_/333246", "title"=>"Phylogenies of single-copy genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-27 00:54:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/662824"], "description"=>"<p>Categorization in Eastern and Western United States regions was determined by geographical origin to the east or west of the Mississippi River. Region assignment for each isolate can be found in <b><a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0001573#pntd.0001573.s006\" target=\"_blank\">Table S1</a></b>.</p>*<p>Mixed infections are excluded from these statistics.</p>†<p>NYC STD clinic samples are present in the table as a separate region and are also included in the Eastern United States region.</p>‡<p>Allelic richness is calculated for a minimum sample size of four diploid individuals.</p>§<p>All Indian isolates had the same genotype, most likely due to cross-contamination during <i>in vitro</i> culture of the isolates cultured in the same lab over many years. India is considered as a sample size of one in all subsequent analyses.</p>", "links"=>[], "tags"=>["isolates", "genotyped", "21", "microsatellite"], "article_id"=>333307, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistics_of_all_T_vaginalis_isolates_genotyped_at_21_microsatellite_loci_/333307", "title"=>"Statistics of all <i>T. vaginalis</i> isolates genotyped at 21 microsatellite loci.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-27 00:55:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/662868"], "description"=>"<p><b>A.</b> The number of positive isolates out of the total number tested for each discrete correlate is shown, and partitioned according to whether those isolates are type 1 or type 2. <b>B.</b> The mean and median value for the total number (N) of isolates tested for several continuous correlates is shown, and partitioned according to whether those parasites are type 1 or type 2. All available clinical data were included in the analyses and specific analytical methods are indicated in parentheses.</p>*<p>indicates statistical significance.</p>", "links"=>[], "tags"=>["types"], "article_id"=>333348, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlations_between_T_vaginalis_types_and_clinical_phenotypes_/333348", "title"=>"Correlations between <i>T. vaginalis</i> types and clinical phenotypes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-27 00:55:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/662907"], "description"=>"<p>The number of vaginal swabs collected at each clinic is shown, followed by the number of swabs found to be positive for <i>T. vaginalis</i> by wet mount, <i>in vitro</i> culture and PCR. NA: technician not available at clinic for wet-mount diagnosis during duration of sample collection.</p>*<p>n represents the number of samples diagnosed as positive via wet mount, and N represents the number of samples tested by wet mount. Type 1 parasites are more likely to be infected with the <i>T. vaginalis</i> virus TVV and are more susceptible to metronidazole, compared to type 2 parasites.</p>", "links"=>[], "tags"=>["women", "attending", "york", "std"], "article_id"=>333381, "categories"=>["Infectious Diseases", "Evolutionary Biology"], "users"=>["Melissa D. Conrad", "Andrew W. Gorman", "Julia A. Schillinger", "Pier Luigi Fiori", "Rossana Arroyo", "Nancy Malla", "Mohan Lal Dubey", "Jorge Gonzalez", "Susan Blank", "William E. Secor", "Jane M. Carlton"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0001573.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prevalence_of_T_vaginalis_in_women_attending_New_York_City_STD_clinics_/333381", "title"=>"Prevalence of <i>T. vaginalis</i> in women attending New York City STD clinics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-27 00:56:21"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"18", "full-text"=>"23", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
  • {"unique-ip"=>"23", "full-text"=>"12", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"15", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
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  • {"unique-ip"=>"23", "full-text"=>"27", "pdf"=>"20", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"24", "full-text"=>"27", "pdf"=>"12", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"12", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"20", "full-text"=>"21", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"40", "full-text"=>"41", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"33", "full-text"=>"38", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"23", "full-text"=>"27", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"21", "full-text"=>"29", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
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Relative Metric

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