Infection with Helicobacter pylori Is Associated with Protection against Tuberculosis
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{"title"=>"Infection with Helicobacter pylori is associated with protection against tuberculosis", "type"=>"journal", "authors"=>[{"first_name"=>"Sharon", "last_name"=>"Perry", "scopus_author_id"=>"10139046800"}, {"first_name"=>"Bouke C.", "last_name"=>"De Jong", "scopus_author_id"=>"8863850000"}, {"first_name"=>"Jay V.", "last_name"=>"Solnick", "scopus_author_id"=>"7003318024"}, {"first_name"=>"Maria", "last_name"=>"De La Luz Sanchez", "scopus_author_id"=>"8633813100"}, {"first_name"=>"Shufang", "last_name"=>"Yang", "scopus_author_id"=>"7406945046"}, {"first_name"=>"Philana Ling", "last_name"=>"Lin", "scopus_author_id"=>"7403225471"}, {"first_name"=>"Lori M.", "last_name"=>"Hansen", "scopus_author_id"=>"7401576023"}, {"first_name"=>"Najeeha", "last_name"=>"Talat", "scopus_author_id"=>"23391057700"}, {"first_name"=>"Philip C.", "last_name"=>"Hill", "scopus_author_id"=>"12779383000"}, {"first_name"=>"Rabia", "last_name"=>"Hussain", "scopus_author_id"=>"7103224786"}, {"first_name"=>"Richard A.", "last_name"=>"Adegbola", "scopus_author_id"=>"7006296329"}, {"first_name"=>"Jo Anne", "last_name"=>"Flynn", "scopus_author_id"=>"7403246739"}, {"first_name"=>"Don", "last_name"=>"Canfield", "scopus_author_id"=>"7101619077"}, {"first_name"=>"Julie", "last_name"=>"Parsonnet", "scopus_author_id"=>"7005136877"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"77649316035", "doi"=>"10.1371/journal.pone.0008804", "pui"=>"358404152", "issn"=>"19326203", "pmid"=>"20098711", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "scopus"=>"2-s2.0-77649316035"}, "id"=>"ff8aab73-627f-3c2e-a6f3-7bf391f0d5b6", "abstract"=>"BACKGROUND: Helicobacter pylori, a lifelong and typically asymptomatic infection of the stomach, profoundly alters gastric immune responses, and may benefit the host in protection against other pathogens. We explored the hypothesis that H. pylori contributes to the control of infection with Mycobacterium tuberculosis.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: We first examined M. tuberculosis-specific IFN-gamma and H. pylori antibody responses in 339 healthy Northern Californians undergoing routine tuberculin skin testing. Of 97 subjects (29%) meeting criteria for latent tuberculosis (TB) infection (LTBI), 45 (46%) were H. pylori seropositive. Subjects with LTBI who were H. pylori-seropositive had 1.5-fold higher TB antigen-induced IFN-gamma responses (p = 0.04, ANOVA), and a more Th-1 like cytokine profile in peripheral blood mononuclear cells, compared to those who were H. pylori seronegative. To explore an association between H. pylori infection and clinical outcome of TB exposure, we evaluated H. pylori seroprevalence in baseline samples from two high risk TB case-contact cohorts, and from cynomolgus macaques experimentally challenged with M. tuberculosis. Compared to 513 household contacts who did not progress to active disease during a median 24 months follow-up, 120 prevalent TB cases were significantly less likely to be H. pylori infected (AOR: 0.55, 95% CI 0.0.36-0.83, p = 0.005), though seroprevalence was not significantly different from non-progressors in 37 incident TB cases (AOR: 1.35 [95% CI 0.63-2.9] p = 0.44). Cynomolgus macaques with natural H. pylori infection were significantly less likely to progress to TB 6 to 8 months after M. tuberculosis challenge (RR: 0.31 [95% CI 0.12-0.80], p = 0.04).\\n\\nCONCLUSIONS/SIGNIFICANCE: H. pylori infection may induce bystander effects that modify the risk of active TB in humans and non-human primates. That immunity to TB may be enhanced by exposure to other microbial agents may have important implications for vaccine development and disease control.", "link"=>"http://www.mendeley.com/research/infection-helicobacter-pylori-associated-protection-against-tuberculosis-5", "reader_count"=>79, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>5, "Other"=>8, "Student > Master"=>4, "Student > Bachelor"=>10, "Lecturer"=>3, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>3, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>19, "Student > Postgraduate"=>5, "Other"=>8, "Student > Master"=>4, "Student > Bachelor"=>10, "Lecturer"=>3, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>30, "Medicine and Dentistry"=>19, "Arts and Humanities"=>2, "Design"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Business, Management and Accounting"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>8}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>19}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>8}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>30}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>9}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>2, "Japan"=>1, "United Kingdom"=>1, "Germany"=>1, "India"=>1, "Spain"=>1, "Russia"=>1}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/430374", "https://ndownloader.figshare.com/files/430403", "https://ndownloader.figshare.com/files/430451", "https://ndownloader.figshare.com/files/430484", "https://ndownloader.figshare.com/files/430523", "https://ndownloader.figshare.com/files/430561", "https://ndownloader.figshare.com/files/430591"], "description"=>"<div><h3>Background</h3><p><em>Helicobacter pylori</em>, a lifelong and typically asymptomatic infection of the stomach, profoundly alters gastric immune responses, and may benefit the host in protection against other pathogens. We explored the hypothesis that <em>H. pylori</em> contributes to the control of infection with <em>Mycobacterium tuberculosis</em>.</p><h3>Methodology/Principal Findings</h3><p>We first examined <em>M. tuberculosis</em>-specific IFN-γ and <em>H. pylori</em> antibody responses in 339 healthy Northern Californians undergoing routine tuberculin skin testing. Of 97 subjects (29%) meeting criteria for latent tuberculosis (TB) infection (LTBI), 45 (46%) were <em>H. pylori</em> seropositive. Subjects with LTBI who were <em>H. pylori</em>-seropositive had 1.5-fold higher TB antigen-induced IFN-γ responses (<em>p = 0.04</em>, ANOVA), and a more Th-1 like cytokine profile in peripheral blood mononuclear cells, compared to those who were <em>H. pylori</em> seronegative. To explore an association between <em>H. pylori</em> infection and clinical outcome of TB exposure, we evaluated <em>H. pylori</em> seroprevalence in baseline samples from two high risk TB case-contact cohorts, and from cynomolgus macaques experimentally challenged with <em>M. tuberculosis</em>. Compared to 513 household contacts who did not progress to active disease during a median 24 months follow-up, 120 prevalent TB cases were significantly less likely to be <em>H. pylori</em> infected (AOR: 0.55, 95% CI 0.0.36–0.83, <em>p = 0.005</em>), though seroprevalence was not significantly different from non-progressors in 37 incident TB cases (AOR: 1.35 [95% CI 0.63–2.9] <em>p = 0.44</em>). Cynomolgus macaques with natural <em>H. pylori</em> infection were significantly less likely to progress to TB 6 to 8 months after <em>M. tuberculosis</em> challenge (RR: 0.31 [95% CI 0.12–0.80], <em>p = 0.04</em>).</p><h3>Conclusions/Significance</h3><p><em>H. pylori</em> infection may induce bystander effects that modify the risk of active TB in humans and non-human primates. That immunity to TB may be enhanced by exposure to other microbial agents may have important implications for vaccine development and disease control.</p></div>", "links"=>[], "tags"=>["tuberculosis"], "article_id"=>144948, "categories"=>["Immunology", "Biological Sciences", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.s001", "https://dx.doi.org/10.1371/journal.pone.0008804.s002", "https://dx.doi.org/10.1371/journal.pone.0008804.s003", "https://dx.doi.org/10.1371/journal.pone.0008804.s004", "https://dx.doi.org/10.1371/journal.pone.0008804.s005", "https://dx.doi.org/10.1371/journal.pone.0008804.s006", "https://dx.doi.org/10.1371/journal.pone.0008804.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Infection_with_Helicobacter_pylori_Is_Associated_with_Protection_against_Tuberculosis/144948", "title"=>"Infection with <em>Helicobacter pylori</em> Is Associated with Protection against Tuberculosis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-01-20 01:22:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/866888"], "description"=>"<p>Blood samples were recruited for <i>H. pylori</i> serology testing from the specimen banks of tuberculosis case- contact studies carried out in (<b>A</b>) The Gambia, West Africa (Ref. 13,16), and (<b>B</b>) Karachi, Pakistan (Ref 14). Each study followed household members exposed to an active (index) case of tuberculosis for at least 2 years. Eligible samples were from HIV-negative participants. Samples from Gambia were randomly selected in 2 groups to match household contacts by age and sex to index and incident TB cases, respectively. <i>LTBI</i>: latent tuberculosis infection at baseline, defined as TST ≥10mm or ELISPOT ≥8 SFU (Gambia), or as TST ≥10mm (Pakistan). Baseline characteristics are shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0008804#pone.0008804.s004\" target=\"_blank\">Table S4</a>.</p>", "links"=>[], "tags"=>["recruited", "tuberculosis", "case-contact"], "article_id"=>537327, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Samples_recruited_for_H_pylori_testing_from_Tuberculosis_Case_Contact_Studies_/537327", "title"=>"Samples recruited for <i>H. pylori</i> testing from Tuberculosis Case-Contact Studies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-20 02:02:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/867024"], "description"=>"<p><b>A</b>: TB antigen induced (24 hour) IFN-γ responses in 97 subjects classified as TB infected [LTBI] and 242 subjects classified as without LTBI, stratified by <i>H. pylori</i> infection status; <i>p-values</i> denote age and sex-adjusted difference within LTBI classification (ANOVA). <b>B.</b> panel A obtained by substituting results of Hepatitis A virus total IgG antibody response [HAV] for <i>H. pylori</i> response; <b>C.</b> mean IFN-γ levels within 97 LTBI+ by <i>H. pylori</i> and HAV antibody test results; <i>p-values</i> denote contrast within each infection grouping. LTBI+: TST≥10 mm induration or QuantiFERON-TB GOLD® positive (≥0.35 IU/ml difference over unstimulated well); LTBI−: TST<10mm and QuantiFERON-TB GOLD®-<0.35 IU/ml; <i>error bars</i> represent 95% confidence interval of the least squares means.</p>", "links"=>[], "tags"=>["responses", "tb", "antigens", "amplified", "concurrently", "infected"], "article_id"=>537461, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IFN_947_responses_to_TB_antigens_are_amplified_in_concurrently_infected_subjects_/537461", "title"=>"IFN<i>-γ</i> responses to TB antigens are amplified in concurrently infected subjects.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-20 02:04:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/867116"], "description"=>"<p><b>A.</b> Scatterplot of principal component scores for 40 adults with latent TB infection (either QuantiFERON-TB GOLD® or TST positive) obtained after linear transformation with eigenvector coefficients. <i>Vertical-axis</i>: 1<sup>st</sup> component (eigenvalue 2.6), which is largely explained by IFN-γ and IL-2, and to a lesser extent IP-10 and TNF-α. <i>Horizontal axis:</i> 2nd PC (eigenvalue 1.5), characterized by loading of IL-13 and IL-5 and negative correlations with the four inflammatory markers. <i>Red circles:</i> 23 <i>H. pylori</i> infected; <i>Black circles:</i> 17 <i>H. pylori</i> seronegative. Reference lines denote quadrants centered on 0; <b>B.</b> comparison of median composite Th1 and Th2 component scores; <i>p-values</i> computed by Wilcoxon's 2-sided median test.</p>", "links"=>[], "tags"=>["immunology/immunity to infections", "infectious diseases/gastrointestinal infections", "infectious diseases/respiratory infections", "public health and epidemiology/infectious diseases"], "article_id"=>537558, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Concurrent_H_pylori_infection_is_associated_with_Th1_Th2_8722_type_profile_/537558", "title"=>"Concurrent <i>H. pylori</i> infection is associated with Th1<sup>+</sup>/Th2<sup>−</sup> type profile.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-01-20 02:05:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/867191"], "description"=>"<p>Characteristics of healthy individuals referred through public health clinics in Santa Clara County, CA, USA who completed tuberculin skin test [TST], QuantiFERON-TB GOLD® interferon-γ release assay, and <i>H. pylori</i> serology.</p>1<p>152 (91%) born in Latin America; TST: tuberculin skin test, +, ≥ 10mm induration (includes 18 prior positives not retested); QFT (QuantiFERON-TB-GOLD® including <i>M. tuberculosis</i> antigens ESAT6 and CFP10 and <i>M. tuberculosis</i> antigen TB7.7; +: ≥0.35 IU/ml IFN-γ difference over unstimulated well.</p>2<p>Latent TB infection [LTBI]: either TST+ or QFT+ for analysis; 7 (2%) individuals reported prophylactic TB treatment 3–34 years prior to enrollment. All factors significant at p<0.05 (2-sided χ<sup>2</sup> test).</p>", "links"=>[], "tags"=>["california"], "article_id"=>537640, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Population_characteristics_Northern_California_H_pylori_LTBI_studies_/537640", "title"=>"Population characteristics: Northern California <i>H. pylori</i>/LTBI studies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-20 02:07:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/867249"], "description"=>"<p><i>Nonprogressor</i>: household contact of TB case remaining disease free at least 2 years from baseline; <i>Prevalent (Index) case</i>: untreated active TB case at baseline; <i>Incident TB case:</i> household contact developing active TB 3–49 months from baseline (<i>see methods).; H.L.:</i> Hosmer-Lemeshow test.</p>", "links"=>[], "tags"=>["caga", "tuberculosis", "case-contact", "cohort", "samples"], "article_id"=>537685, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Factors_associated_with_H_pylori_CagA_infection_in_tuberculosis_case_contact_cohort_samples_adjusted_odds_ratio_/537685", "title"=>"Factors associated with <i>H. pylori</i> CagA infection in tuberculosis case-contact cohort samples (<i>adjusted odds ratio</i>).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-20 02:08:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/867294"], "description"=>"<p>Seroprevalence of <i>H. pylori</i> infection in 41 Pittsburgh cynomolgus macaques by outcome of TB challenge at 6–8 months.</p>", "links"=>[], "tags"=>["41", "pittsburgh", "cynomolgus", "macaques", "tb"], "article_id"=>537736, "categories"=>["Immunology", "Computational Biology", "Engineering", "Medicine"], "users"=>["Sharon Perry", "Bouke C. de Jong", "Jay V. Solnick", "Maria de la Luz Sanchez", "Shufang Yang", "Philana Ling Lin", "Lori M. Hansen", "Najeeha Talat", "Philip C. Hill", "Rabia Hussain", "Richard A. Adegbola", "JoAnne Flynn", "Don Canfield", "Julie Parsonnet"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008804.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Seroprevalence_of_H_pylori_infection_in_41_Pittsburgh_cynomolgus_macaques_by_outcome_of_TB_challenge_at_6_8_months_/537736", "title"=>"Seroprevalence of <i>H. pylori</i> infection in 41 Pittsburgh cynomolgus macaques by outcome of TB challenge at 6–8 months.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-01-20 02:08:56"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"21", "full-text"=>"25", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
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  • {"unique-ip"=>"24", "full-text"=>"25", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"33", "full-text"=>"36", "pdf"=>"9", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"7", "cited-by"=>"3", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"24", "full-text"=>"26", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
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  • {"unique-ip"=>"29", "full-text"=>"28", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"24", "full-text"=>"24", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"15", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
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  • {"unique-ip"=>"66", "full-text"=>"62", "pdf"=>"284", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"7", "cited-by"=>"2", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"33", "full-text"=>"42", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
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Relative Metric

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