Prior Population Immunity Reduces the Expected Impact of CTL-Inducing Vaccines for Pandemic Influenza Control
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{"title"=>"Prior population immunity reduces the expected impact of CTL-inducing vaccines for pandemic influenza control", "type"=>"journal", "authors"=>[{"first_name"=>"Kirsty J.", "last_name"=>"Bolton", "scopus_author_id"=>"54998702900"}, {"first_name"=>"James M.", "last_name"=>"McCaw", "scopus_author_id"=>"21735020500"}, {"first_name"=>"Lorena", "last_name"=>"Brown", "scopus_author_id"=>"7404220474"}, {"first_name"=>"David", "last_name"=>"Jackson", "scopus_author_id"=>"13003942900"}, {"first_name"=>"Katherine", "last_name"=>"Kedzierska", "scopus_author_id"=>"8374461700"}, {"first_name"=>"Jodie", "last_name"=>"McVernon", "scopus_author_id"=>"6701712603"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203", "sgr"=>"84926299762", "pui"=>"603466622", "scopus"=>"2-s2.0-84926299762", "issn"=>"19326203", "pmid"=>"25811654", "doi"=>"10.1371/journal.pone.0120138"}, "id"=>"05923cf5-491c-3d67-9900-1ee08202cd9b", "abstract"=>"Vaccines that trigger an influenza-specific cytotoxic T cell (CTL) response may aid pandemic control by limiting the transmission of novel influenza A viruses (IAV). We consider interventions with hypothetical CTL-inducing vaccines in a range of epidemiologically plausible pandemic scenarios. We estimate the achievable reduction in the attack rate, and, by adopting a model linking epidemic progression to the emergence of IAV variants, the opportunity for antigenic drift. We demonstrate that CTL-inducing vaccines have limited utility for modifying population-level outcomes if influenza-specific T cells found widely in adults already suppress transmission and prove difficult to enhance. Administration of CTL-inducing vaccines that are efficacious in \"influenza-experienced\" and \"influenza-naive\" hosts can likely slow transmission sufficiently to mitigate a moderate IAV pandemic. However if neutralising cross-reactive antibody to an emerging IAV are common in influenza-experienced hosts, as for the swine-variant H3N2v, boosting CTL immunity may be ineffective at reducing population spread, indicating that CTL-inducing vaccines are best used against novel subtypes such as H7N9. Unless vaccines cannot readily suppress transmission from infected hosts with naive T cell pools, targeting influenza-naive hosts is preferable. Such strategies are of enhanced benefit if naive hosts are typically intensively mixing children and when a subset of experienced hosts have pre-existing neutralising cross-reactive antibody. We show that CTL-inducing vaccination campaigns may have greater power to suppress antigenic drift than previously suggested, and targeting adults may be the optimal strategy to achieve this when the vaccination campaign does not have the power to curtail the attack rate. Our results highlight the need to design interventions based on pre-existing cellular immunity and knowledge of the host determinants of vaccine efficacy, and provide a framework for assessing the performance requirements of high-impact CTL-inducing vaccines.", "link"=>"http://www.mendeley.com/research/prior-population-immunity-reduces-expected-impact-ctlinducing-vaccines-pandemic-influenza-control", "reader_count"=>16, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Mathematics"=>2, "Medicine and Dentistry"=>6, "Agricultural and Biological Sciences"=>2, "Psychology"=>2, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Psychology"=>{"Psychology"=>2}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>2}}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1991054", "https://ndownloader.figshare.com/files/1991055", "https://ndownloader.figshare.com/files/1991056", "https://ndownloader.figshare.com/files/1991057", "https://ndownloader.figshare.com/files/1991058", "https://ndownloader.figshare.com/files/1991059", "https://ndownloader.figshare.com/files/1991060", "https://ndownloader.figshare.com/files/1991061", "https://ndownloader.figshare.com/files/1991062", "https://ndownloader.figshare.com/files/1991063"], "description"=>"<div><p>Vaccines that trigger an influenza-specific cytotoxic T cell (CTL) response may aid pandemic control by limiting the <i>transmission</i> of novel influenza A viruses (IAV). We consider interventions with hypothetical CTL-inducing vaccines in a range of epidemiologically plausible pandemic scenarios. We estimate the achievable reduction in the attack rate, and, by adopting a model linking epidemic progression to the emergence of IAV variants, the opportunity for antigenic drift. We demonstrate that CTL-inducing vaccines have limited utility for modifying population-level outcomes if influenza-specific T cells found widely in adults already suppress transmission and prove difficult to enhance. Administration of CTL-inducing vaccines that are efficacious in \"influenza-experienced\" and \"influenza-naive\" hosts can likely slow transmission sufficiently to mitigate a moderate IAV pandemic. However if neutralising cross-reactive antibody to an emerging IAV are common in influenza-experienced hosts, as for the swine-variant H3N2v, boosting CTL immunity may be ineffective at reducing population spread, indicating that CTL-inducing vaccines are best used against novel subtypes such as H7N9. Unless vaccines cannot readily suppress transmission from infected hosts with naive T cell pools, targeting influenza-naive hosts is preferable. Such strategies are of enhanced benefit if naive hosts are typically intensively mixing children and when a subset of experienced hosts have pre-existing neutralising cross-reactive antibody. We show that CTL-inducing vaccination campaigns may have greater power to suppress antigenic drift than previously suggested, and targeting adults may be the optimal strategy to achieve this when the vaccination campaign does not have the power to curtail the attack rate. Our results highlight the need to design interventions based on pre-existing cellular immunity and knowledge of the host determinants of vaccine efficacy, and provide a framework for assessing the performance requirements of high-impact CTL-inducing vaccines.</p></div>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357792, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0120138.s001", "https://dx.doi.org/10.1371/journal.pone.0120138.s002", "https://dx.doi.org/10.1371/journal.pone.0120138.s003", "https://dx.doi.org/10.1371/journal.pone.0120138.s004", "https://dx.doi.org/10.1371/journal.pone.0120138.s005", "https://dx.doi.org/10.1371/journal.pone.0120138.s006", "https://dx.doi.org/10.1371/journal.pone.0120138.s007", "https://dx.doi.org/10.1371/journal.pone.0120138.s008", "https://dx.doi.org/10.1371/journal.pone.0120138.s009", "https://dx.doi.org/10.1371/journal.pone.0120138.s010"], "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prior_Population_Immunity_Reduces_the_Expected_Impact_of_CTL_Inducing_Vaccines_for_Pandemic_Influenza_Control_/1357792", "title"=>"Prior Population Immunity Reduces the Expected Impact of CTL-Inducing Vaccines for Pandemic Influenza Control", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991052"], "description"=>"<p>Drift opportunity for scenario C with targeted distribution of a vaccine stockpile sufficient for 50 per cent coverage and assuming that pre-vaccination <i>R</i><sub>eff</sub> = 2. The axis labelled <i>ϵ</i><sub>v</sub> indicates the relative infectiousness of vaccinated and unvaccinated naïve hosts and “exp coverage” indicates the fractional vaccine coverage in experienced hosts (vaccine distribution is random when exp coverage is 0.5). Each panel corresponds to a different assumption regarding the form for the per infection rate of antigenic emergence <i>g</i><sub>0,<i>i</i></sub>; equal probability per infection (<i>left</i>), proportional to host infectiousness (<i>middle</i>), and zero for vaccinated hosts with existing CTL protection (<i>right</i>). The vertical axis show the probability of emergence <i>P</i><sub>emg</sub> of an antigenically novel variant over the course of the epidemic relative to the same scenario without intervention.</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357790, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.g005", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Drift_opportunity_in_scenario_C_/1357790", "title"=>"Drift opportunity in scenario C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991051"], "description"=>"<p><b>Upper panels:</b> drift opportunity relative to an unimpeded epidemic as a function of general population coverage for four different pandemic and vaccine action scenarios assuming <i>R</i><sub>eff</sub> = 2, homogeneous mixing and <i>g</i><sub>0,<i>i</i></sub> = 1. <b>Lower panels:</b> The ratio of effective reproduction numbers of antigenically novel and resident pandemic variants. The grey line indicates a ratio of unity. In each panel the solid line indicates results assuming that the relative infectiousness in vaccinated naïve and naïve hosts is <i>ϵ</i><sub>v</sub> = 0.25, with dashed and dotted lines <i>ϵ</i><sub>v</sub> = 0.5 and 0.75 respectively.</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357789, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.g004", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Drift_opportunity_with_coverage_for_scenarios_A_D_/1357789", "title"=>"Drift opportunity with coverage for scenarios A-D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991050"], "description"=>"<p>Epidemic attack rates for targeted distribution of a vaccine stockpile sufficient for 50 per cent coverage. For all epidemics the initial effective reproduction number in the absence of vaccination is fixed at 2. The axis labelled “exp coverage” denotes coverage in the experienced population and <i>ϵ</i><sub>v</sub> is the relative infectiousness of vaccinated and unvaccinated naïve hosts. The minimum plotted value of “exp coverage” indicates full coverage in the naïve population with the remainder given to experienced hosts, the maximum plotted value is for a scenario in which all vaccines are given to experienced hosts, and a value of 0.5 indicates equal coverage in naïve and experienced hosts (<i>i.e.</i> general population distribution). Panels represent estimates for different pre-pandemic immunity and vaccine action scenarios; 80 per cent of the population with naturally acquired CTL-mediated immunity (<i>f</i><sub><i>E</i></sub> = 0.8) and saturating vaccine action (scenario B), the same population with a vaccine that boosts protection in all hosts (scenario C), a population in which 50 per cent of those with naturally acquired CTL responses also have protective antibody to the pandemic strain and vaccine action is again boosting (scenario D). The strength of naturally acquired CTL-mediated immunity is set to <i>ϵ</i> = 0.5.</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357788, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Attack_rates_for_targeted_vaccination_in_Scenario_C_/1357788", "title"=>"Attack rates for targeted vaccination in Scenario C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991047"], "description"=>"<p>Predicted attack rates for four different pandemic and vaccine action scenarios as a function of general population coverage with a CTL-inducing vaccine. In each panel the solid line corresponds to assumptions of relative infectiousness in vaccinated and unvaccinated naïve hosts of <i>ϵ</i><sub>v</sub> = 0.25, with dashed and dotted lines corresponding to <i>ϵ</i><sub>v</sub> = 0.5 and 0.75 respectively. Scenario A captures a population without pre-existing CTL-mediated immunity to the pandemic strain. In scenarios B and C, 80 per cent of the population have pre-existing CTL-mediated immunity (<i>f</i><sub><i>E</i></sub> = 0.8) suppressing infectiousness by 50 per cent (<i>ϵ</i> = 0.5), with vaccine action saturating (B) or boosting (C). Scenario D is a modification of scenario C that assumes 50 per cent of those with naturally acquired CTL immunity also have cross-reactive protective antibody.</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357785, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Attack_rate_with_coverage_for_scenarios_A_D_/1357785", "title"=>"Attack rate with coverage for scenarios A-D.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991045"], "description"=>"<p>Susceptible hosts are divided into 4 strata (labelled by <i>i</i>) depending on their prior influenza experience and vaccination status. Susceptible hosts <i>S</i><sub><i>i</i></sub> become exposed (<i>E</i><sub><i>i</i></sub>) at a rate proportional to <i>β</i><sub><i>f</i></sub>, become infectious (<i>I</i><sub><i>i</i></sub>) with Erlang distributed waiting time with rate parameter <i>γ</i> = 1/(1.3 days) and recover (<i>R</i><sub><i>i</i></sub>) at a rate <i>ν</i> = 1/(1.6 days). Dashed lines indicate the vaccination of hosts. Note we assume that vaccines do not alter the infectiousness of already exposed hosts (although this distinction is of little consequence if vaccination occurs very early in a pandemic). We allow for the possibility of strain-specific antibody to the pandemic strain by assuming that some (experienced) hosts begin in the recovered state <i>R</i><sub>3</sub>. We assume infected-acquired immunity is maintained over the course of the simulation, however in practice as immunity wanes recovered hosts who were originally naïve migrate to the appropriate <i>experienced</i> susceptible state (<i>R</i><sub>1</sub> → <i>R</i><sub>4</sub>, <i>R</i><sub>2</sub> → <i>R</i><sub>3</sub>).</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357783, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.g001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_structure_/1357783", "title"=>"Model structure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-26 04:54:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1991053"], "description"=>"<p>The infectiousness of vaccinated and/or experienced hosts (relative to unvaccinated naïve hosts) for the four scenarios A–D presented in the main text. <i>ϵ</i><sub>v</sub> is a free parameter that is set to determine the infectiousness of vaccinated naïve hosts relative to unvaccinated naïve hosts.</p>", "links"=>[], "tags"=>["antigenic drift", "iav", "3n", "host", "vaccine", "pandemic", "ctl", "7N", "Pandemic Influenza Control Vaccines", "attack rate", "T cell pools"], "article_id"=>1357791, "categories"=>["Biological Sciences"], "users"=>["Kirsty J. Bolton", "James M. McCaw", "Lorena Brown", "David Jackson", "Katherine Kedzierska", "Jodie McVernon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0120138.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scenarios_/1357791", "title"=>"Scenarios.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-03-26 04:54:47"}

PMC Usage Stats | Further Information

  • {"unique-ip"=>"25", "full-text"=>"26", "pdf"=>"11", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"23", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"5"}
  • {"unique-ip"=>"15", "full-text"=>"22", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"13", "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"=>"10"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"20", "full-text"=>"15", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"6", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"2", "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"=>"4", "full-text"=>"2", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"4"}
  • {"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"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
  • {"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"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"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"=>"11"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"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"=>"2017", "month"=>"4"}
  • {"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"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "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"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"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"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"2", "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"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"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"=>"9"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"8", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"11", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"3", "full-text"=>"1", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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