One Is Enough: In Vivo Effective Population Size Is Dose-Dependent for a Plant RNA Virus
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{"title"=>"One is enough: In vivo effective population size is dose-dependent for a plant RNA virus", "type"=>"journal", "authors"=>[{"first_name"=>"Mark P.", "last_name"=>"Zwart", "scopus_author_id"=>"23037708900"}, {"first_name"=>"José Antonio", "last_name"=>"Daròs", "scopus_author_id"=>"6602841633"}, {"first_name"=>"Santiago F.", "last_name"=>"Elena", "scopus_author_id"=>"7006364449"}], "year"=>2011, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-79960939505", "sgr"=>"79960939505", "pui"=>"362246992", "isbn"=>"1553-7374", "pmid"=>"21750676", "doi"=>"10.1371/journal.ppat.1002122"}, "id"=>"11620843-56b1-3917-bf4b-1f01f53bd2f6", "abstract"=>"Effective population size (N(e)) determines the strength of genetic drift and the frequency of co-infection by multiple genotypes, making it a key factor in viral evolution. Experimental estimates of N(e) for different plant viruses have, however, rendered diverging results. The independent action hypothesis (IAH) states that each virion has a probability of infection, and that virions act independent of one another during the infection process. A corollary of IAH is that N(e) must be dose dependent. A test of IAH for a plant virus has not been reported yet. Here we perform a test of an IAH infection model using a plant RNA virus, Tobacco etch virus (TEV) variants carrying GFP or mCherry fluorescent markers, in Nicotiana tabacum and Capsicum annuum plants. The number of primary infection foci increased linearly with dose, and was similar to a Poisson distribution. At high doses, primary infection foci containing both genotypes were found at a low frequency (<2%). The probability that a genotype that infected the inoculated leaf would systemically infect that plant was near 1, although in a few rare cases genotypes could be trapped in the inoculated leaf by being physically surrounded by the other genotype. The frequency of mixed-genotype infection could be predicted from the mean number of primary infection foci using the independent-action model. Independent action appears to hold for TEV, and N(e) is therefore dose-dependent for this plant RNA virus. The mean number of virions causing systemic infection can be very small, and approaches 1 at low doses. Dose-dependency in TEV suggests that comparison of N(e) estimates for different viruses are not very meaningful unless dose effects are taken into consideration.", "link"=>"http://www.mendeley.com/research/one-enough-vivo-effective-population-size-dosedependent-plant-rna-virus-4", "reader_count"=>8, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>2, "Other"=>1, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>2, "Other"=>1, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>2, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/758312"], "description"=>"<p>The ordinate is the mean ln-transformed number of foci of primary infection plus one, with error bars indicating 95% confidence intervals, while the abscise is ln-transformed dose (the number of virions per inoculated plant, as estimated by the number of RNA molecules measured by RT-qPCR). The orange circles and blue squares are data points for <i>N. tabacum</i> and <i>C. annuum</i>, respectively. The orange and blue lines are the fitted IAH dose-foci relationship. A good model fit for <i>N. tabacum</i> (<i>R</i><sup>2</sup> = 0.713, <i>F</i><sub>1,21</sub> = 52.091, <i>P</i><0.001) and <i>C. annuum</i> (<i>R</i><sup>2</sup> = 0.799, <i>F</i><sub>1,12</sub> = 47.636, <i>P</i><0.001) indicates number of foci increase linearly with dose. Note that the data and model taper off as the mean number of foci becomes low due to the ln transformation.</p>", "links"=>[], "tags"=>["foci", "inoculated", "leaves"], "article_id"=>428685, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Number_of_primary_infection_foci_in_inoculated_leaves_at_different_doses_/428685", "title"=>"Number of primary infection foci in inoculated leaves at different doses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:24:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/758694"], "description"=>"<p>All panels are merges of red and green fluorescence observed in <i>N. tabacum</i> plants inoculated with TEV-GFP and TEV-mCherry. Panel A is the only TEV-mCherry primary infection focus observed in the inoculated leaf, which at 132 hpi is surrounded by TEV-GFP and tissue damaged by the inoculation. Note that vascular tissue is present directly below the focus, but that only the TEV-GFP virus is visible there. In B, a view of systemically infected leaves is shown. No red fluorescence was seen in systemically infected leaves, indicating TEV-mCherry was trapped in the primary infection focus. In Panel C is the only green fluorescence observed in another plant. Although the TEV-GFP virus appears to have spread locally in the inoculated leaf, it is entirely surrounded by TEV-mCherry, and no green fluorescence was visible in systemically infected leaves (Panel D). Although these observations represent a mechanism of dependence between virions in the infection process (antagonism), ‘trapping’ of one of the two viruses in the inoculated leaf was observed only in 1.8% of the infected <i>N. tabacum</i> plants.</p>", "links"=>[], "tags"=>["dependence", "virions"], "article_id"=>429073, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_mechanism_of_dependence_between_virions_during_infection_of_N_tabacum_/429073", "title"=>"A mechanism of dependence between virions during infection of <i>N. tabacum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:31:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/758603"], "description"=>"<p>Plants were infected with 1∶30 dilution of a mixture of amplified TEV-GFP and TEV-mCherry virions, kept on ice for 0 h (panel A), 2 h (panel B) or 3 h (panel C). Yellow, mixed-genotype foci were observed at low frequency at all three time points (1.8% averaged for all three times), and the frequency of mixed-genotype foci did not change significantly over time (test for a trend in proportions: χ<sup>2</sup> = 0.041, 1 d.f., <i>P</i> = 0.839). Plants were also infected with a 1∶10 dilution of the same mixture (Panel D): the number of mixed-genotype foci may be higher, but these leaves could not be quantitatively scored. High magnification pictures of yellow foci are also provided (Panels E and F). Note that the distribution of red and green fluorescence is not homogeneous within yellow foci.</p>", "links"=>[], "tags"=>["foci", "inoculated"], "article_id"=>428978, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mixed_genotype_foci_of_primary_infection_in_the_inoculated_leaf_/428978", "title"=>"Mixed-genotype foci of primary infection in the inoculated leaf.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:29:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/758952"], "description"=>"<p>Dilution is the dilution of the purified virions used to inoculate plants, and virion dose is the number of virions per inoculated plant, as estimated by the number of RNA molecules measured by RT-qPCR. Mean foci is the mean number of foci of primary infection, of both TEV-GFP and TEV-mCherry, in an inoculated leaf. Variance is the calculated variance of the mean number of foci of primary infection. Note that for a Poisson distribution, the mean is equal to the variance. We test this expectation with a one-sample Kolmogorov-Smirnoff (KS) test. <i>Z</i> is the KS test statistic, and <i>P</i> its significance. Not a single test remained significant after applying the conservative Holm-Bonferroni correction for multiple tests of the same null hypothesis. The variance appears to deviate more from the mean at high doses, however. N.D. indicates data were not determined for a particular replicate and dose.</p>", "links"=>[], "tags"=>["foci"], "article_id"=>429340, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variance_in_the_mean_number_of_foci_of_primary_infection_for_N_tabacum_/429340", "title"=>"Variance in the mean number of foci of primary infection for <i>N. tabacum</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-07 02:35:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/758894"], "description"=>"<p><i>P</i> values are the significance level of the corresponding one-sample <i>t</i>-test for the null hypothesis <i>κ</i> = 1. Asterisks indicate cases that remain significant after the more stringent Holm-Bonferroni correction.</p>", "links"=>[], "tags"=>["fitting"], "article_id"=>429273, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.t003", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Parameters_estimated_for_the_fitting_of_the_dose_response_general_infection_model_to_each_dataset_/429273", "title"=>"Parameters estimated for the fitting of the dose response general infection model to each dataset.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-07 02:34:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/758179"], "description"=>"<p>The development of foci of primary infection in the inoculated leaf of <i>N. tabacum</i> was followed over time. Patterns in vascular tissue, observed under visible light through a stereomicroscope (‘Plant A: Vis.’), were used to track fluorescence in the same region. GFP and mCherry signals were merged, and given for three example plants (‘Plant A: Fluo.’ through ‘Plant C: Fluo.’). The best time point for viewing foci of primary infection is 84 hpi: the foci have reasonably high levels of fluorescence, but the fluorescence has not spread.</p>", "links"=>[], "tags"=>["inoculated"], "article_id"=>428554, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g001", "stats"=>{"downloads"=>3, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fluorescence_time_course_in_inoculated_N_tabacum_leaves_/428554", "title"=>"Fluorescence time course in inoculated <i>N. tabacum</i> leaves.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:22:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/758795"], "description"=>"<p>In panel A, the inoculated leaf of a <i>C. annuum</i> plant is shown. Note the areas of the leaf damaged due to inoculation. In panel B, the same region of the leaf is shown but with merged GFP and mCherry signal. mCherry is restricted to small portion of the leaf, probably also in part due to leaf damage from inoculation. On day three, there were three mCherry foci visible in the inoculated leaf. Note that the yellow signal in this panel is due to leaf damage, and not co-infection of tissue. In panel C, the rest of the plant is shown, and only GFP signal is present. TEV-mCherry has therefore been ‘trapped’ in the inoculated leaf. This exclusion was observed in only one infected <i>C. annuum</i> plant (0.9%).</p>", "links"=>[], "tags"=>["virions"], "article_id"=>429174, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dependence_of_virions_during_infection_of_C_annuum_/429174", "title"=>"Dependence of virions during infection of <i>C. annuum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/758377"], "description"=>"<p>The rate of infection and mixed-genotype infection predicted from the number of primary infection foci in the inoculated leaf.</p>", "links"=>[], "tags"=>["mixed-genotype", "foci", "inoculated"], "article_id"=>428751, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.g003", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_rate_of_infection_and_mixed_genotype_infection_predicted_from_the_number_of_primary_infection_foci_in_the_inoculated_leaf_/428751", "title"=>"The rate of infection and mixed-genotype infection predicted from the number of primary infection foci in the inoculated leaf.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-07-07 02:25:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/381502", "https://ndownloader.figshare.com/files/381544"], "description"=>"<div><p>Effective population size (<em>N<sub>e</sub></em>) determines the strength of genetic drift and the frequency of co-infection by multiple genotypes, making it a key factor in viral evolution. Experimental estimates of <em>N<sub>e</sub></em> for different plant viruses have, however, rendered diverging results. The independent action hypothesis (IAH) states that each virion has a probability of infection, and that virions act independent of one another during the infection process. A corollary of IAH is that <em>N<sub>e</sub></em> must be dose dependent. A test of IAH for a plant virus has not been reported yet. Here we perform a test of an IAH infection model using a plant RNA virus, <em>Tobacco etch virus</em> (TEV) variants carrying GFP or mCherry fluorescent markers, in <em>Nicotiana tabacum</em> and <em>Capsicum annuum</em> plants. The number of primary infection foci increased linearly with dose, and was similar to a Poisson distribution. At high doses, primary infection foci containing both genotypes were found at a low frequency (<2%). The probability that a genotype that infected the inoculated leaf would systemically infect that plant was near 1, although in a few rare cases genotypes could be trapped in the inoculated leaf by being physically surrounded by the other genotype. The frequency of mixed-genotype infection could be predicted from the mean number of primary infection foci using the independent-action model. Independent action appears to hold for TEV, and <em>N<sub>e</sub></em> is therefore dose-dependent for this plant RNA virus. The mean number of virions causing systemic infection can be very small, and approaches 1 at low doses. Dose-dependency in TEV suggests that comparison of <em>N<sub>e</sub></em> estimates for different viruses are not very meaningful unless dose effects are taken into consideration.</p> </div>", "links"=>[], "tags"=>["dose-dependent", "rna"], "article_id"=>135364, "categories"=>["Cancer", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002122.s001", "https://dx.doi.org/10.1371/journal.ppat.1002122.s002"], "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/One_Is_Enough_In_Vivo_Effective_Population_Size_Is_Dose_Dependent_for_a_Plant_RNA_Virus/135364", "title"=>"One Is Enough: <em>In Vivo</em> Effective Population Size Is Dose-Dependent for a Plant RNA Virus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-07-07 01:29:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/758923"], "description"=>"<p>Dilution is the dilution of the purified virions used to inoculate plants, and virion dose is the number of virions per inoculated plant, as estimated by the number of RNA molecules measured by RT-qPCR. Mean foci is the mean number of foci of primary infection, of both TEV-GFP and TEV-mCherry, in an inoculated leaf. Variance is the calculated variance of the mean number of foci of primary infection. Note that for a Poisson distribution, the mean is equal to the variance. We test this expectation with a one-sample Kolmogorov-Smirnoff (KS) test. <i>Z</i> is the KS test statistic, and <i>P</i> its significance. Not a single test remained significant after applying the conservative Holm-Bonferroni correction for multiple tests of the same null hypothesis. N.D. indicates data were not determined for a particular replicate and dose.</p>", "links"=>[], "tags"=>["foci"], "article_id"=>429298, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variance_in_the_mean_number_of_foci_of_primary_infection_for_C_annuum_/429298", "title"=>"Variance in the mean number of foci of primary infection for <i>C. annuum</i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-07 02:34:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/758865"], "description"=>"<p>TS stands for ‘this study’. RE stands for restriction enzyme. The experimental setups were classified according to which part of the transmission or infection process was considered for <i>N<sub>e</sub></i> was estimated: I. Full transmission process: systemic leaf – vector – inoculated leaf – systemic leaf. II. Partial infection process: inoculum - inoculated leaf. III. Partial infection process: inoculated leaf – systemic leaf. Doses are given as the number of RNA molecules measured in purified virions stocks for data from this study, or as ng of purified virions per inoculated plant for study <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002122#ppat.1002122-Sacristan1\" target=\"_blank\">[30]</a>. <i>N<sub>e</sub></i> estimates are given with the standard error of the mean, or the reported range of estimates. Estimates of <i>N<sub>e</sub></i> are made for (systemically) infected hosts, with the exception of those estimates marked with an asterisk (*) which are estimates made over the whole host population, not only the infected hosts.</p>a<p>Only data from the wild-type/P20L experiment presented, as other experiments with other genotype combinations gave highly similar results.</p>b<p><i>N<sub>e</sub></i> estimates made for different mixtures of an infective and non-infective genotype used, leading to different levels of infection. The mean level of infection is given.</p>c<p>The estimated number of virions transmitted per aphid; 2 aphids per plant were used in the study.</p>d<p>The mean number of genotypes found in infected plants is given, which is a rough approximation of <i>N<sub>e</sub></i> as the number of genotypes used (12) is much higher than the number of genotypes found in infected plants.</p>e<p>F1F2F3 and F1L2F3 genotypes.</p>f<p>F1F2F3 and F1L2F3 genotypes, and satellite.</p>", "links"=>[], "tags"=>["estimates"], "article_id"=>429241, "categories"=>["Virology", "Ecology", "Microbiology", "Evolutionary Biology"], "users"=>["Mark P. Zwart", "José-Antonio Darós", "Santiago F. Elena"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002122.t004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_estimates_of_N_e_/429241", "title"=>"Comparison of estimates of <i>N<sub>e</sub></i>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-07-07 02:34:01"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"18", "full-text"=>"14", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"11", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"4", "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"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "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"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"2", "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"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"1", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"2", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"28", "full-text"=>"34", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"11", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

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