The Synthetic Plasmodium falciparum Circumsporozoite Peptide PfCS102 as a Malaria Vaccine Candidate: A Randomized Controlled Phase I Trial
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{"title"=>"The synthetic Plasmodium falciparum circumsporozoite peptide PfCS102 as a malaria vaccine candidate: A randomized controlled phase I trial", "type"=>"journal", "authors"=>[{"first_name"=>"Régine", "last_name"=>"Audran", "scopus_author_id"=>"7004585055"}, {"first_name"=>"Floriana", "last_name"=>"Lurati-Ruiz", "scopus_author_id"=>"14422514300"}, {"first_name"=>"Blaise", "last_name"=>"Genton", "scopus_author_id"=>"35501901200"}, {"first_name"=>"Hildur E.", "last_name"=>"Blythman", "scopus_author_id"=>"57191134209"}, {"first_name"=>"Opokua", "last_name"=>"Ofori-Anyinam", "scopus_author_id"=>"8571271900"}, {"first_name"=>"Christophe", "last_name"=>"Reymond", "scopus_author_id"=>"7004618720"}, {"first_name"=>"Giampietro", "last_name"=>"Corradin", "scopus_author_id"=>"7006737733"}, {"first_name"=>"François", "last_name"=>"Spertini", "scopus_author_id"=>"7006111987"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"19798415", "doi"=>"10.1371/journal.pone.0007304", "sgr"=>"70350135532", "isbn"=>"1932-6203 (Electronic)", "scopus"=>"2-s2.0-70350135532", "issn"=>"19326203", "pui"=>"355440957"}, "id"=>"b198c9d6-42fe-37c8-8532-277b6fdb58cd", "abstract"=>"BACKGROUND: Fully efficient vaccines against malaria pre-erythrocytic stage are still lacking. The objective of this dose/adjuvant-finding study was to evaluate the safety, reactogenicity and immunogenicity of a vaccine candidate based on a peptide spanning the C-terminal region of Plasmodium falciparum circumsporozoite protein (PfCS102) in malaria naive adults.\\n\\nMETHODOLOGY AND PRINCIPAL FINDINGS: Thirty-six healthy malaria-naive adults were randomly distributed into three dose blocks (10, 30 and 100 microg) and vaccinated with PfCS102 in combination with either Montanide ISA 720 or GSK proprietary Adjuvant System AS02A at days 0, 60, and 180. Primary end-point (safety and reactogenicity) was based on the frequency of adverse events (AE) and of abnormal biological safety tests; secondary-end point (immunogenicity) on P. falciparum specific cell-mediated immunity and antibody response before and after immunization. The two adjuvant formulations were well tolerated and their safety profile was good. Most AEs were local and, when systemic, involved mainly fatigue and headache. Half the volunteers in AS02A groups experienced severe AEs (mainly erythema). After the third injection, 34 of 35 volunteers developed anti-PfCS102 and anti-sporozoite antibodies, and 28 of 35 demonstrated T-cell proliferative responses and IFN-gamma production. Five of 22 HLA-A2 and HLA-A3 volunteers displayed PfCS102 specific IFN-gamma secreting CD8(+) T cell responses. Responses were only marginally boosted after the 3(rd) vaccination and remained stable for 6 months. For both adjuvants, the dose of 10 microg was less immunogenic in comparison to 30 and 100 microg that induced similar responses. AS02A formulations with 30 microg or 100 microg PfCS102 induced about 10-folds higher antibody and IFN-gamma responses than Montanide formulations.\\n\\nCONCLUSIONS/SIGNIFICANCE: PfCS102 peptide was safe and highly immunogenic, allowing the design of more advanced trials to test its potential for protection. Two or three immunizations with a dose of 30 microg formulated with AS02A appeared the most appropriate choice for such studies.\\n\\nTRIAL REGISTRATION: Swissmedic.ch 2002 DR 1227.", "link"=>"http://www.mendeley.com/research/synthetic-plasmodium-falciparum-circumsporozoite-peptide-pfcs102-malaria-vaccine-candidate-randomize", "reader_count"=>25, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>3}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>8, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>1, "Nursing and Health Professions"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Computer Science"=>{"Computer Science"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>1, "France"=>1, "Spain"=>1}, "group_count"=>5}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/881970"], "description"=>"<p>Values indicate numbers of volunteers presenting an individual increase in frequency of IFN-γ secreting PfCS102 specific CD4<sup>+</sup> or CD8<sup>+</sup> T cells, i.e. with an induced frequency above the mean + 95% confidence interval of the pre-immune specific responses in the 22 HLA-A2 and/or HLA-A3 volunteers and a delta above 0.02%.</p>", "links"=>[], "tags"=>["producing", "responses", "peptide", "injection", "adjuvant"], "article_id"=>552418, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.t004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_IFN_producing_CD4_and_CD8_T_cell_responses_based_on_the_dose_of_peptide_per_injection_or_the_adjuvant_used_/552418", "title"=>"Analysis of IFN-γ producing CD4<sup>+</sup> and CD8<sup>+</sup> T cell responses based on the dose of peptide per injection or the adjuvant used.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-10-02 00:40:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/881460"], "description"=>"<p>Proliferative responses were evaluated by <sup>3</sup>[H]-thymidine incorporation by peripheral blood mononuclear cells (PBMC) upon stimulation with antigen. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007304#s3\" target=\"_blank\">Results</a> are expressed as individual stimulation indices (SI) in each immunization group with quartiles. Arrows indicate the times of vaccination.</p>", "links"=>[], "tags"=>["anti-pfcs102", "proliferative"], "article_id"=>551908, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_anti_PfCS102_proliferative_T_cell_response_/551908", "title"=>"Time-course of anti-PfCS102 proliferative T cell response.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:31:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/881619"], "description"=>"<p>IFN-γ was evaluated in the supernatant of stimulated peripheral blood mononuclear cells (PBMC). <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007304#s3\" target=\"_blank\">Results</a> are expressed as individual IFN-γ secretion, expressed in pg/ml for each immunization group, with quartiles. Arrows indicate the times of vaccination.</p>", "links"=>[], "tags"=>["pbmc"], "article_id"=>552072, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_the_IFN_947_production_by_PBMC_in_response_to_PfCS102_/552072", "title"=>"Time-course of the IFN-γ production by PBMC in response to PfCS102.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:34:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/881755"], "description"=>"<p>Frequencies were evaluated by intracellular cytokine staining (ICS) using the PBMC of HLA-A2 and/or HLA-A3 volunteers. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007304#s3\" target=\"_blank\">Results</a> are expressed as percentage of IFN-γ positive cells upon PfCS stimulation in the selected cell population: A, CD4<sup>+</sup> cells; B, CD8<sup>+</sup> cells; C, CD3<sup>+</sup>CD8<sup>+</sup> T cells (CD16<sup>−</sup>/56<sup>−</sup>, CTL, and CD16<sup>+</sup>/56<sup>+</sup>, NKT cells) in 8 responders. Dotted lines represent baseline. Statistical analysis was based on Wilcoxon's test with <i>p</i><0.05 as the limit of significance. Arrows indicate the times of vaccination.</p>", "links"=>[], "tags"=>["frequencies", "pfcs102"], "article_id"=>552204, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_individual_frequencies_of_PfCS102_specific_T_cells_/552204", "title"=>"Time-course of individual frequencies of PfCS102 specific T cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:36:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/880862"], "description"=>"<p>Design of the Phase I, double-blind, dose-ranging study of 3 vaccine dosing regimens combined to two different adjuvants AS02A and Montanide ISA 720. For each dose, volunteers were randomized by blocks of 12, with 6 individuals per adjuvant. Volunteers were seen 2 and 30 d after the first injection, 2 and 15 d after the second injection and 2, 15, 180, and 360 d after the third injection. A phone call was addressed to all volunteers at d 30 after the 2<sup>nd</sup> and 3<sup>rd</sup> injection.</p>", "links"=>[], "tags"=>["immunology/immune response", "immunology/immunity to infections", "infectious diseases/protozoal infections", "infectious diseases/tropical and travel-associated diseases", "public health and epidemiology/immunization"], "article_id"=>551309, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Study_flow_chart_/551309", "title"=>"Study flow chart.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:21:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/881853"], "description"=>"<p>Data are numbers of participants presenting with symptoms. n: number of participants per analysis group. M: Montanide ISA 720. A: AS02A. Gr.3: grade 3.</p>", "links"=>[], "tags"=>["adverse", "events", "4-day", "follow-up"], "article_id"=>552302, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.t002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Local_adverse_events_during_the_4_day_follow_up_after_each_immunization_/552302", "title"=>"Local adverse events during the 4-day follow-up after each immunization.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-10-02 00:38:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/881899"], "description"=>"<p>Data are numbers of participants presenting with symptoms. n: number of participants per group. M: Montanide ISA 720. A: AS02A. GI: gastrointestinal troubles. Gr.3: grade 3.</p>§<p>Other solicited adverse events included dizziness (n = 6), sweating (n = 5), dyspnea (n = 3), exanthema, palpitations, hand erythema (n = 1).</p>", "links"=>[], "tags"=>["systemic", "adverse", "events", "4-day", "follow-up"], "article_id"=>552346, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.t003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Solicited_systemic_adverse_events_during_the_4_day_follow_up_after_each_immunization_/552346", "title"=>"Solicited systemic adverse events during the 4-day follow-up after each immunization.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-10-02 00:39:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/881283"], "description"=>"<p>Anti-parasite antibodies were measured in plasma samples by immunofluorescence. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007304#s3\" target=\"_blank\">Results</a> are expressed as individual titers for each immunization group, with quartiles. Arrows indicate the times of vaccination.</p>", "links"=>[], "tags"=>["antibody", "pfcs102"], "article_id"=>551733, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_anti_Plasmodium_falciparum_antibody_response_upon_PfCS102_immunization_/551733", "title"=>"Time-course of anti-<i>Plasmodium falciparum</i> antibody response upon PfCS102 immunization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:28:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/436826", "https://ndownloader.figshare.com/files/436900", "https://ndownloader.figshare.com/files/437080", "https://ndownloader.figshare.com/files/437221", "https://ndownloader.figshare.com/files/437293"], "description"=>"<div><h3>Background</h3><p>Fully efficient vaccines against malaria pre-erythrocytic stage are still lacking. The objective of this dose/adjuvant-finding study was to evaluate the safety, reactogenicity and immunogenicity of a vaccine candidate based on a peptide spanning the C-terminal region of <em>Plasmodium falciparum</em> circumsporozoite protein (PfCS102) in malaria naive adults.</p><h3>Methodology and Principal Findings</h3><p>Thirty-six healthy malaria-naive adults were randomly distributed into three dose blocks (10, 30 and 100 µg) and vaccinated with PfCS102 in combination with either Montanide ISA 720 or GSK proprietary Adjuvant System AS02A at days 0, 60, and 180. Primary end-point (safety and reactogenicity) was based on the frequency of adverse events (AE) and of abnormal biological safety tests; secondary-end point (immunogenicity) on <em>P. falciparum</em> specific cell-mediated immunity and antibody response before and after immunization. The two adjuvant formulations were well tolerated and their safety profile was good. Most AEs were local and, when systemic, involved mainly fatigue and headache. Half the volunteers in AS02A groups experienced severe AEs (mainly erythema). After the third injection, 34 of 35 volunteers developed anti-PfCS102 and anti-sporozoite antibodies, and 28 of 35 demonstrated T-cell proliferative responses and IFN-γ production. Five of 22 HLA-A2 and HLA-A3 volunteers displayed PfCS102 specific IFN-γ secreting CD8<sup>+</sup> T cell responses. Responses were only marginally boosted after the 3<sup>rd</sup> vaccination and remained stable for 6 months. For both adjuvants, the dose of 10 µg was less immunogenic in comparison to 30 and 100 µg that induced similar responses. AS02A formulations with 30 µg or 100 µg PfCS102 induced about 10-folds higher antibody and IFN-γ responses than Montanide formulations.</p><h3>Conclusions/Significance</h3><p>PfCS102 peptide was safe and highly immunogenic, allowing the design of more advanced trials to test its potential for protection. Two or three immunizations with a dose of 30 µg formulated with AS02A appeared the most appropriate choice for such studies.</p><h3>Trial Registration</h3><p>Swissmedic.ch 2002 DR 1227</p></div>", "links"=>[], "tags"=>["synthetic", "circumsporozoite", "peptide", "pfcs102", "malaria", "randomized", "controlled"], "article_id"=>146138, "categories"=>["Medicine", "Immunology", "Cancer", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0007304.s001", "https://dx.doi.org/10.1371/journal.pone.0007304.s002", "https://dx.doi.org/10.1371/journal.pone.0007304.s003", "https://dx.doi.org/10.1371/journal.pone.0007304.s004", "https://dx.doi.org/10.1371/journal.pone.0007304.s005"], "stats"=>{"downloads"=>13, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Synthetic_Plasmodium_falciparum_Circumsporozoite_Peptide_PfCS102_as_a_Malaria_Vaccine_Candidate_A_Randomized_Controlled_Phase_I_Trial/146138", "title"=>"The Synthetic <em>Plasmodium falciparum</em> Circumsporozoite Peptide PfCS102 as a Malaria Vaccine Candidate: A Randomized Controlled Phase I Trial", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-10-02 01:42:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/881130"], "description"=>"<p>Anti-PfCS102 antibodies were measured in plasma samples by ELISA. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007304#s3\" target=\"_blank\">Results</a> are expressed as individual data in U/ml for each immunization group, with quartiles. Arrows indicate the times of vaccination.</p>", "links"=>[], "tags"=>["anti-pfcs102", "antibody", "pfcs102"], "article_id"=>551581, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.g002", "stats"=>{"downloads"=>4, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_anti_PfCS102_antibody_response_upon_PfCS102_immunization_/551581", "title"=>"Time course of anti-PfCS102 antibody response upon PfCS102 immunization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-10-02 00:26:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/881929"], "description"=>"<p>Characteristics of participants in various immunization groups.</p>", "links"=>[], "tags"=>["immunization"], "article_id"=>552382, "categories"=>["Medicine", "Immunology", "Infectious Diseases", "Physics"], "users"=>["Regine Audran", "Floriana Lurati-Ruiz", "Blaise Genton", "Hildur E. Blythman", "Opokua Ofori-Anyinam", "Christophe Reymond", "Giampietro Corradin", "François Spertini"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007304.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characteristics_of_participants_in_various_immunization_groups_/552382", "title"=>"Characteristics of participants in various immunization groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-10-02 00:39:42"}

PMC Usage Stats | Further Information

  • {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"26", "unique-ip"=>"21", "pdf"=>"6", "year"=>"2010", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"4", "year"=>"2010", "pdf"=>"3", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"1"}
  • {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"12", "unique-ip"=>"16", "pdf"=>"11", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"9", "year"=>"2010", "pdf"=>"9", "unique-ip"=>"10", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"33", "unique-ip"=>"25", "pdf"=>"22", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"3"}
  • {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"10", "year"=>"2010", "pdf"=>"9", "unique-ip"=>"16", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"17", "unique-ip"=>"20", "pdf"=>"16", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"7", "year"=>"2010", "pdf"=>"5", "unique-ip"=>"11", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"10", "unique-ip"=>"12", "pdf"=>"7", "year"=>"2010", "figure"=>"4", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"4", "full-text"=>"13", "year"=>"2010", "pdf"=>"7", "unique-ip"=>"16", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"4", "unique-ip"=>"5", "pdf"=>"0", "year"=>"2010", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"5", "year"=>"2010", "pdf"=>"6", "unique-ip"=>"9", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"15", "unique-ip"=>"25", "pdf"=>"8", "year"=>"2011", "figure"=>"8", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"10", "year"=>"2011", "pdf"=>"4", "unique-ip"=>"19", "figure"=>"9", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"16", "unique-ip"=>"21", "pdf"=>"10", "year"=>"2011", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"9", "year"=>"2011", "pdf"=>"3", "unique-ip"=>"12", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"1"}
  • {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"7", "unique-ip"=>"6", "pdf"=>"3", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"2"}
  • {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"9", "year"=>"2011", "pdf"=>"6", "unique-ip"=>"10", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"1"}
  • {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"4", "pdf"=>"2", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"2", "year"=>"2011", "pdf"=>"5", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "unique-ip"=>"4", "pdf"=>"3", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2011", "pdf"=>"1", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"16", "unique-ip"=>"15", "pdf"=>"9", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2011", "pdf"=>"2", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "unique-ip"=>"2", "pdf"=>"4", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"3", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2012", "pdf"=>"1", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"3", "pdf"=>"2", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
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Relative Metric

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