Major Depletion of Plasmacytoid Dendritic Cells in HIV-2 Infection, an Attenuated Form of HIV Disease
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{"title"=>"Major depletion of plasmacytoid dendritic cells in HIV-2 infection, an attenuated form of HIV disease", "type"=>"journal", "authors"=>[{"first_name"=>"Rita", "last_name"=>"Cavaleiro", "scopus_author_id"=>"18533820700"}, {"first_name"=>"António P.", "last_name"=>"Baptista", "scopus_author_id"=>"57196624381"}, {"first_name"=>"Rui S.", "last_name"=>"Soares", "scopus_author_id"=>"15137293300"}, {"first_name"=>"Rita", "last_name"=>"Tendeiro", "scopus_author_id"=>"26431171300"}, {"first_name"=>"Russell B.", "last_name"=>"Foxall", "scopus_author_id"=>"6701559470"}, {"first_name"=>"Perpétua", "last_name"=>"Gomes", "scopus_author_id"=>"12241342900"}, {"first_name"=>"Rui M.M.", "last_name"=>"Victorino", "scopus_author_id"=>"7005391596"}, {"first_name"=>"Ana E.", "last_name"=>"Sousa", "scopus_author_id"=>"7202484563"}], "year"=>2009, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-73549098013", "sgr"=>"73549098013", "issn"=>"15537366", "doi"=>"10.1371/journal.ppat.1000667", "pmid"=>"19936055", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pui"=>"358060452"}, "id"=>"7e34d3e2-6b8c-3718-b3a5-399601fbaa32", "abstract"=>"Plasmacytoid dendritic cells (pDC) provide an important link between innate and acquired immunity, mediating their action mainly through IFN-alpha production. pDC suppress HIV-1 replication, but there is increasing evidence suggesting they may also contribute to the increased levels of cell apoptosis and pan-immune activation associated with disease progression. Although having the same clinical spectrum, HIV-2 infection is characterized by a strikingly lower viremia and a much slower rate of CD4 decline and AIDS progression than HIV-1, irrespective of disease stage. We report here a similar marked reduction in circulating pDC levels in untreated HIV-1 and HIV-2 infections in association with CD4 depletion and T cell activation, in spite of the undetectable viremia found in the majority of HIV-2 patients. Moreover, the same overexpression of CD86 and PD-L1 on circulating pDC was found in both infections irrespective of disease stage or viremia status. Our observation that pDC depletion occurs in HIV-2 infected patients with undetectable viremia indicates that mechanisms other than direct viral infection determine the pDC depletion during persistent infections. However, viremia was associated with an impairment of IFN-alpha production on a per pDC basis upon TLR9 stimulation. These data support the possibility that diminished function in vitro may relate to prior activation by HIV virions in vivo, in agreement with our finding of higher expression levels of the IFN-alpha inducible gene, MxA, in HIV-1 than in HIV-2 individuals. Importantly, serum IFN-alpha levels were not elevated in HIV-2 infected individuals. In conclusion, our data in this unique natural model of \"attenuated\" HIV immunodeficiency contribute to the understanding of pDC biology in HIV/AIDS pathogenesis, showing that in the absence of detectable viremia a major depletion of circulating pDC in association with a relatively preserved IFN-alpha production does occur.", "link"=>"http://www.mendeley.com/research/major-depletion-plasmacytoid-dendritic-cells-hiv2-infection-attenuated-form-hiv-disease", "reader_count"=>48, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>12, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>6, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>12, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>16, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Psychology"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>16}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "France"=>1, "Portugal"=>1}, "group_count"=>0}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/875939"], "description"=>"<p>Freshly isolated PBMC were cultured in the absence or in the presence of CpG. After 22 hours, culture supernatants were harvested and analyzed for the secretion of IL-10, IL-12p40, MIP-1β and TNF-α using the Luminex multiplex assay. (<b>A</b>) Cytokine levels. Each dot represents one individual. The levels observed in non-stimulated cultures (open symbols) are connected with those documented in the presence of CpG (closed symbols), and were compared using Wilcoxon test. (<b>B</b>) Stimulation indexes defined as ratio between the level of cytokine in the supernatant of the culture in the presence of CpG and in its absence (medium) in the three cohorts. (<b>C</b>) The HIV-2 and the HIV-1 cohorts were split according to the presence of detectable and undectable viremia and the stimulation indexes for TNF-α are shown. Bars represent mean±SEM. Numbers under the bars represent the total individuals analyzed. The subgroups of patients analyzed are representative of their respective patient population described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000667#ppat-1000667-t001\" target=\"_blank\">Table 1</a> with respect to CD4 counts and viral load. The Mann-Whitney test was used to compare the data of the HIV-2, HIV-1 and healthy cohorts, and the significant p values (<0.05) are shown.</p>", "links"=>[], "tags"=>["levels", "cpg", "stimulation", "hiv-1", "hiv-2"], "article_id"=>546381, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g006", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IL_10_IL_12p40_MIP_1_946_and_TNF_945_levels_upon_CpG_stimulation_in_Healthy_HIV_1_and_HIV_2_cohorts_/546381", "title"=>"IL-10, IL-12p40, MIP-1β and TNF-α levels upon CpG stimulation in Healthy, HIV-1 and HIV-2 cohorts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:46:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/875356"], "description"=>"<p>A representative flow cytometric pDC analysis is shown in (<b>A</b>). After a large gate including lymphocytes and monocytes defined by forward and side scatter, cells were further gated on HLA-DR<sup>+</sup> cells that do not express lineage markers (left dot-plot). pDC were subsequently identified as CD123<sup>+</sup>CD11c<sup>−</sup> cells (right dot-plot). Numbers represent the percentage of cells within the illustrated gates from an HIV-2 infected patient with 523 CD4 T cell/µl and undetectable viremia. The proportion of pDC within PBMC is 0.15% corresponding to 4 pDC/µl. (<b>B</b>) Graphs show circulating pDC levels in HIV-1 and HIV-2 infected cohorts and healthy controls expressed as percentage within PBMC and absolute numbers. Each dot represents one individual and bars represent mean. (<b>C</b>) The infected cohorts were stratified according to CD4 T cell counts (>350 and <350 cells/µl) and pDC levels compared as percentages and absolute numbers. Bars represent mean±SEM. Numbers under the bars represent the total individuals analyzed. <sup>*</sup>p<0.05, <sup>**</sup>p<0.01 and <sup>***</sup>p<0.001 as compared to pDC levels in controls. <sup>#</sup>p<0.05 between early and advanced HIV-2 cohorts.</p>", "links"=>[], "tags"=>["circulating", "pdc", "hiv-1", "hiv-2"], "article_id"=>545790, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Similar_reduction_of_circulating_pDC_in_HIV_1_and_HIV_2_infections_/545790", "title"=>"Similar reduction of circulating pDC in HIV-1 and HIV-2 infections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:36:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/875599"], "description"=>"<p>(<b>A</b>) Phenotype of circulating pDC in HIV-1 and HIV-2 infections. Levels of expression of CD86 and PD-L1 on pDC from freshly isolated PBMC assessed as proportion within pDC and as geomean FI within total pDC measured by flow cytometry. Each dot represents one individual and bars represent mean. (<b>B</b>) pDC phenotype upon CpG stimulation. Freshly isolated PBMC were cultured with medium alone, CpG or the non-CpG ODN control. pDC phenotype was assessed by flow cytometry after 22 hours. Histograms represent the analysis of CD40 and CD80 expression upon CpG stimulation within pDC in a representative HIV-2 infected patient with 508 CD4 T cells/µl and 13627 HIV-2 RNA copies/ml. After a large gate including lymphocytes and monocytes defined by forward and side scatter, cells were sequentially gated on HLA-DR<sup>+</sup> cells that do not express lineage markers and on CD123<sup>+</sup>CD11c<sup>−</sup> cells. (<b>C</b>) The up-regulation of CD40 expression on pDC is showed as stimulation index defined as ratio between the geomean FI in the presence of CpG or ODN and in its absence (medium). Data are presented within total HIV-1 and HIV-2 cohorts (left graph) and within the infected cohorts grouped according to viremia status (right graph). Bars represent mean±SEM. Numbers under the bars represent the total HIV-1 and HIV-2 infected individuals as well as healthy controls analyzed. The subgroups of patients analyzed are representative of their respective patient population described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000667#ppat-1000667-t001\" target=\"_blank\">Table 1</a> with respect to CD4 counts and viral load. There are no significant differences between HIV-1 and HIV-2 cohorts. <sup>*</sup>p<0.05, <sup>**</sup>p<0.01 and <sup>***</sup>p<0.001 as compared to controls. <sup>#</sup>p<0.05 between “aviremic” and viremic patients of the HIV-1 cohort.</p>", "links"=>[], "tags"=>["immunology", "immunology/immunity to infections", "immunology/innate immunity", "infectious diseases/hiv infection and aids", "infectious diseases/viral infections", "virology/host antiviral responses", "virology/immunodeficiency viruses"], "article_id"=>546043, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g003", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_pDC_Phenotype_/546043", "title"=>"pDC Phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:40:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/875486"], "description"=>"<p>Correlation between percentage of pDC within PBMC and percentage of CD4 T cells (<b>A</b>), percentage of HLA-DR within CD4 T cells (<b>C</b>), as well as percentage of HLA-DR<sup>+</sup>CD38<sup>+</sup> within CD8 T cells (<b>D</b>), in HIV-2 and HIV-1 infections. Comparison of the pDC frequencies in the infected cohorts divided into viremic and “aviremic” (below test cut-off) groups (<b>B</b>). Bars represent mean±SEM. Numbers under the bars represent the total individuals analyzed. <sup>***</sup>p<0.001 as compared to controls. <sup>##</sup>p<0.01 between “aviremic” and viremic patients of the same cohort. <sup>&&</sup>p<0.01 between HIV-1 and HIV-2 “aviremic” patients.</p>", "links"=>[], "tags"=>["pdc", "levels", "cd4", "activation"], "article_id"=>545928, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_of_pDC_levels_with_CD4_T_cell_T_cell_activation_and_viremia_/545928", "title"=>"Relationship of pDC levels with CD4 T cell, T cell activation and viremia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:38:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/875702"], "description"=>"<p>Freshly isolated PBMC were stimulated with CpG or the non-CpG ODN control. After 22 hours IFN-α was quantified in culture supernatants by ELISA. (<b>A</b>) Levels of IFN-α upon CpG or the non-CpG ODN control in healthy, HIV-1 and HIV-2 cohorts. The infected cohorts were further stratified according to CD4 T cell counts (<b>B</b>) or the presence or absence of detectable viremia (<b>C</b>) and the levels of IFN-α upon CpG stimulation are shown. Results expressed as “Net IFN-α” refer to the amount of IFN-α produced upon CpG stimulation subtracted by the IFN-α measured with medium alone. The “Net IFN-α” was divided by the total number of pDC in the culture and results are shown for the healthy, HIV-1 and HIV-2 cohorts (<b>D</b>), as well as for the infected cohorts stratified according to CD4 T cell counts (<b>E</b>) or the presence or absence of detectable viremia (<b>F</b>). Each dot represents one individual. Bars represent mean±SEM. Numbers under the bars represent the total individuals analyzed. The subgroups of patients analyzed are representative of their respective patient population described in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000667#ppat-1000667-t001\" target=\"_blank\">Table 1</a> with respect to CD4 counts and viral load. <sup>**</sup>p<0.01 and <sup>***</sup>p<0.001 as compared to controls. <sup>#</sup>p<0.05 and <sup>##</sup>p<0.01 between the two groups of the same infected cohort. <sup>&</sup> p<0.05 between HIV-1 and HIV-2 patients with more than 350 CD4 T cells/µl.</p>", "links"=>[], "tags"=>["cpg"], "article_id"=>546146, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IFN_945_production_upon_CpG_stimulation_/546146", "title"=>"IFN-α production upon CpG stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:42:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/434061", "https://ndownloader.figshare.com/files/434123"], "description"=>"<div><p>Plasmacytoid dendritic cells (pDC) provide an important link between innate and acquired immunity, mediating their action mainly through IFN-α production. pDC suppress HIV-1 replication, but there is increasing evidence suggesting they may also contribute to the increased levels of cell apoptosis and pan-immune activation associated with disease progression. Although having the same clinical spectrum, HIV-2 infection is characterized by a strikingly lower viremia and a much slower rate of CD4 decline and AIDS progression than HIV-1, irrespective of disease stage. We report here a similar marked reduction in circulating pDC levels in untreated HIV-1 and HIV-2 infections in association with CD4 depletion and T cell activation, in spite of the undetectable viremia found in the majority of HIV-2 patients. Moreover, the same overexpression of CD86 and PD-L1 on circulating pDC was found in both infections irrespective of disease stage or viremia status. Our observation that pDC depletion occurs in HIV-2 infected patients with undetectable viremia indicates that mechanisms other than direct viral infection determine the pDC depletion during persistent infections. However, viremia was associated with an impairment of IFN-α production on a per pDC basis upon TLR9 stimulation. These data support the possibility that diminished function <em>in vitro</em> may relate to prior activation by HIV virions <em>in vivo</em>, in agreement with our finding of higher expression levels of the IFN-α inducible gene, <em>MxA</em>, in HIV-1 than in HIV-2 individuals. Importantly, serum IFN-α levels were not elevated in HIV-2 infected individuals. In conclusion, our data in this unique natural model of “attenuated” HIV immunodeficiency contribute to the understanding of pDC biology in HIV/AIDS pathogenesis, showing that in the absence of detectable viremia a major depletion of circulating pDC in association with a relatively preserved IFN-α production does occur.</p></div>", "links"=>[], "tags"=>["depletion", "plasmacytoid", "dendritic", "cells", "hiv-2", "attenuated", "hiv"], "article_id"=>145643, "categories"=>["Immunology", "Cancer", "Medicine"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000667.s001", "https://dx.doi.org/10.1371/journal.ppat.1000667.s002"], "stats"=>{"downloads"=>6, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Major_Depletion_of_Plasmacytoid_Dendritic_Cells_in_HIV_2_Infection_an_Attenuated_Form_of_HIV_Disease/145643", "title"=>"Major Depletion of Plasmacytoid Dendritic Cells in HIV-2 Infection, an Attenuated Form of HIV Disease", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-11-20 01:34:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/876049"], "description"=>"<p>Relative <i>MxA</i> mRNA expression was quantified by real-time PCR in 10 healthy subjects, 20 HIV-1 and 24 HIV-2 infected patients and expressed as mean±SEM of <i>MxA</i> mRNA copies/1000 GAPDH mRNA copies. Correlations were evaluated in 8 healthy, 17 HIV-1 and 23 HIV-2 individuals, except for Net IFN-α (14 HIV-1 and 17 HIV-2). <sup>#</sup>p = 0.0421 as compared to HIV-2 cohort. NA, not applicable.</p>", "links"=>[], "tags"=>["mrna"], "article_id"=>546498, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_MxA_mRNA_expression_/546498", "title"=>"Relative <i>MxA</i> mRNA expression.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-11-20 01:48:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/875823"], "description"=>"<p>Correlations of frequency of circulating CD4 T cells, proportion of CD4 T cells that express HLA-DR, proportion of CD8 T cells that simultaneously express HLA-DR and CD38, viremia and levels of proviral DNA with the Net IFN-α production (<b>A</b>) and the Net IFN-α per 1000 pDC (<b>B</b>) upon <i>in vitro</i> CpG stimulation. Each dot represents one individual from the HIV-2 cohort, the HIV-1 cohort and healthy controls.</p>", "links"=>[], "tags"=>["cpg", "stimulation", "cd4", "viremia", "proviral", "dna"], "article_id"=>546259, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_of_IFN_945_production_upon_CpG_stimulation_with_CD4_T_cells_T_cell_activation_viremia_and_proviral_DNA_levels_/546259", "title"=>"Relationship of IFN-α production upon CpG stimulation with CD4 T cells, T cell activation, viremia and proviral DNA levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-11-20 01:44:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/876098"], "description"=>"<p>Data are mean±SEM with limits in brackets. NA, not applicable. <sup>#</sup>p<0.05 in comparison with HIV-2 infected patients; <sup>*</sup>p<0.05, <sup>**</sup>p<0.01, <sup>***</sup>p<0.001 in comparison with healthy individuals.<sup> a</sup>n = 17; <sup>b</sup>n = 16; <sup>c</sup>n = 21; <sup>d</sup>4 out of 22 HIV-1 patients and 20 out of 28 HIV-2 patients had undetectable viremia. In these cases, the cut-off value of the test (40 and 200 RNA copies/ml for HIV-1 and HIV-2, respectively) was used to calculate the mean; <sup>e</sup>Proviral DNA was quantified in 21 HIV-1 and 28 HIV-2 infected patients. It was detectable in all the patients evaluated but in 3 cases from the HIV-2 cohort it was below the cut-off value of the test (5 HIV DNA copies/10<sup>6</sup> PBMC copies). In these cases, the cut-off value of the test was used to calculate the mean.</p>", "links"=>[], "tags"=>["cohorts"], "article_id"=>546547, "categories"=>["Immunology", "Infectious Diseases", "Medicine", "Virology"], "users"=>["Rita Cavaleiro", "António P. Baptista", "Rui S. Soares", "Rita Tendeiro", "Russell B. Foxall", "Perpétua Gomes", "Rui M. M. Victorino", "Ana E. Sousa"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000667.t001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characteristics_of_the_cohorts_studied_/546547", "title"=>"Characteristics of the cohorts studied.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-11-20 01:49:07"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
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Relative Metric

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