HIV-1 Superinfection Occurs Less Frequently Than Initial Infection in a Cohort of High-Risk Kenyan Women
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{"title"=>"HIV-1 Superinfection Occurs Less Frequently Than Initial Infection in a Cohort of High-Risk Kenyan Women", "type"=>"journal", "authors"=>[{"first_name"=>"Keshet", "last_name"=>"Ronen", "scopus_author_id"=>"24333023000"}, {"first_name"=>"Connor O.", "last_name"=>"McCoy", "scopus_author_id"=>"55017381900"}, {"first_name"=>"Frederick A.", "last_name"=>"Matsen", "scopus_author_id"=>"35448078400"}, {"first_name"=>"David F.", "last_name"=>"Boyd", "scopus_author_id"=>"55842802100"}, {"first_name"=>"Sandra", "last_name"=>"Emery", "scopus_author_id"=>"7005789547"}, {"first_name"=>"Katherine", "last_name"=>"Odem-Davis", "scopus_author_id"=>"49561770500"}, {"first_name"=>"Walter", "last_name"=>"Jaoko", "scopus_author_id"=>"6602407057"}, {"first_name"=>"Kishor", "last_name"=>"Mandaliya", "scopus_author_id"=>"35427966200"}, {"first_name"=>"R. Scott", "last_name"=>"McClelland", "scopus_author_id"=>"7101803892"}, {"first_name"=>"Barbra A.", "last_name"=>"Richardson", "scopus_author_id"=>"35426099900"}, {"first_name"=>"Julie", "last_name"=>"Overbaugh", "scopus_author_id"=>"7005063858"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-84883414441", "sgr"=>"84883414441", "issn"=>"15537366", "doi"=>"10.1371/journal.ppat.1003593", "pmid"=>"24009513", "isbn"=>"1553-7366", "pui"=>"369735811"}, "id"=>"a636ed0a-e844-3cd9-944a-74e9d45ee48a", "abstract"=>"HIV superinfection (reinfection) has been reported in several settings, but no study has been designed and powered to rigorously compare its incidence to that of initial infection. Determining whether HIV infection reduces the risk of superinfection is critical to understanding whether an immune response to natural HIV infection is protective. This study compares the incidence of initial infection and superinfection in a prospective seroincident cohort of high-risk women in Mombasa, Kenya. A next-generation sequencing-based pipeline was developed to screen 129 women for superinfection. Longitudinal plasma samples at <6 months, >2 years and one intervening time after initial HIV infection were analyzed. Amplicons in three genome regions were sequenced and a median of 901 sequences obtained per gene per timepoint. Phylogenetic evidence of polyphyly, confirmed by pairwise distance analysis, defined superinfection. Superinfection timing was determined by sequencing virus from intervening timepoints. These data were combined with published data from 17 additional women in the same cohort, totaling 146 women screened. Twenty-one cases of superinfection were identified for an estimated incidence rate of 2.61 per 100 person-years (pys). The incidence rate of initial infection among 1910 women in the same cohort was 5.75 per 100 pys. Andersen-Gill proportional hazards models were used to compare incidences, adjusting for covariates known to influence HIV susceptibility in this cohort. Superinfection incidence was significantly lower than initial infection incidence, with a hazard ratio of 0.47 (CI 0.29-0.75, p = 0.0019). This lower incidence of superinfection was only observed >6 months after initial infection. This is the first adequately powered study to report that HIV infection reduces the risk of reinfection, raising the possibility that immune responses to natural infection are partially protective. The observation that superinfection risk changes with time implies a window of protection that coincides with the maturation of HIV-specific immunity.", "link"=>"http://www.mendeley.com/research/hiv1-superinfection-occurs-less-frequently-initial-infection-cohort-highrisk-kenyan-women", "reader_count"=>39, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Mathematics"=>2, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>5, "Business, Management and Accounting"=>1, "Physics and Astronomy"=>2, "Social Sciences"=>3, "Computer Science"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Social Sciences"=>{"Social Sciences"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Hungary"=>1, "United States"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1185018"], "description"=>"<p>Boxplots of pairwise amino acid distances in each genomic region are displayed, comparing the distance between the initial and superinfecting sequences within each superinfection case (red) to the distance between sequences in simulated mixtures of randomly selected pairs of singly-infected individuals (green). <b>A.</b> Analysis of 454 sequences from NGS screen. <b>B.</b> Analysis of 454 sequences from NGS screen and Sanger sequences from 12 previously identified cases of superinfection <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Chohan2\" target=\"_blank\">[5]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Piantadosi1\" target=\"_blank\">[12]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Piantadosi2\" target=\"_blank\">[17]</a>.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "superinfecting"], "article_id"=>784269, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g005", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_similarity_between_initial_and_superinfecting_variants_/784269", "title"=>"Sequence similarity between initial and superinfecting variants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185014"], "description"=>"<p><b>A.</b> Phylogenetic trees representing viral sequence from all timepoints in each genomic region analyzed. The corresponding posterior probability of monophyly is displayed. Initial variant branches are collapsed and highlighted in blue, superinfecting variant branches in red. Red branch labels mark query sequences from individual QD151 at all timepoints, black labels mark reference sequences. <b>B.</b> Maximum percent pairwise distance (PWD) between sequences within each timepoint listed or across all timepoints (All-tp). The 97.5% confidence limit of the distances observed among viral sequences within known singly infected individuals and the 2.5% confidence limit within simulated mixtures of sequences from two individuals are shown for comparison. Timepoints shown in bold type are the 3 samples originally screened; the rest were subsequently sequenced to specify superinfection timing. <sup>1</sup> PWD within 95% confidence interval observed for single infection. <sup>2</sup> PWD outside 95% confidence interval for single infection and within 95% confidence interval for dual infection. <b>C.</b> Schematic summarizing viral variants detected in each genomic region over time (initial variant depicted in blue, superinfecting variant in red). Viral subtype is indicated.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology"], "article_id"=>784265, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Superinfection_case_QD151_/784265", "title"=>"Superinfection case QD151.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185013"], "description"=>"<p>Overview of NGS superinfection screening pipeline.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "ngs", "superinfection"], "article_id"=>784264, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_NGS_superinfection_screening_pipeline_/784264", "title"=>"Overview of NGS superinfection screening pipeline.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185022", "https://ndownloader.figshare.com/files/1185023", "https://ndownloader.figshare.com/files/1185024", "https://ndownloader.figshare.com/files/1185025", "https://ndownloader.figshare.com/files/1185026"], "description"=>"<div><p>HIV superinfection (reinfection) has been reported in several settings, but no study has been designed and powered to rigorously compare its incidence to that of initial infection. Determining whether HIV infection reduces the risk of superinfection is critical to understanding whether an immune response to natural HIV infection is protective. This study compares the incidence of initial infection and superinfection in a prospective seroincident cohort of high-risk women in Mombasa, Kenya. A next-generation sequencing-based pipeline was developed to screen 129 women for superinfection. Longitudinal plasma samples at <6 months, >2 years and one intervening time after initial HIV infection were analyzed. Amplicons in three genome regions were sequenced and a median of 901 sequences obtained per gene per timepoint. Phylogenetic evidence of polyphyly, confirmed by pairwise distance analysis, defined superinfection. Superinfection timing was determined by sequencing virus from intervening timepoints. These data were combined with published data from 17 additional women in the same cohort, totaling 146 women screened. Twenty-one cases of superinfection were identified for an estimated incidence rate of 2.61 per 100 person-years (pys). The incidence rate of initial infection among 1910 women in the same cohort was 5.75 per 100pys. Andersen-Gill proportional hazards models were used to compare incidences, adjusting for covariates known to influence HIV susceptibility in this cohort. Superinfection incidence was significantly lower than initial infection incidence, with a hazard ratio of 0.47 (CI 0.29–0.75, p = 0.0019). This lower incidence of superinfection was only observed >6 months after initial infection. This is the first adequately powered study to report that HIV infection reduces the risk of reinfection, raising the possibility that immune responses to natural infection are partially protective. The observation that superinfection risk changes with time implies a window of protection that coincides with the maturation of HIV-specific immunity.</p></div>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "superinfection", "occurs", "cohort", "high-risk", "kenyan"], "article_id"=>784273, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003593.s001", "https://dx.doi.org/10.1371/journal.ppat.1003593.s002", "https://dx.doi.org/10.1371/journal.ppat.1003593.s003", "https://dx.doi.org/10.1371/journal.ppat.1003593.s004", "https://dx.doi.org/10.1371/journal.ppat.1003593.s005"], "stats"=>{"downloads"=>10, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_Superinfection_Occurs_Less_Frequently_Than_Initial_Infection_in_a_Cohort_of_High_Risk_Kenyan_Women_/784273", "title"=>"HIV-1 Superinfection Occurs Less Frequently Than Initial Infection in a Cohort of High-Risk Kenyan Women", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185020"], "description"=>"<p>Values shown are median (IQR), unless otherwise specified.</p><p>Data shown were collected at time of entry into each risk set (seroincident cohort enrollment for initial infection risk and initial HIV infection for superinfection risk), except where marked.</p>†<p>at seroincident cohort enrollment.</p>∧<p>Time from seroincident cohort enrollment to censoring, regardless of infection events.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "women", "screened"], "article_id"=>784271, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sociodemographic_and_clinical_characteristics_of_women_at_risk_of_initial_infection_and_screened_for_superinfection_/784271", "title"=>"Sociodemographic and clinical characteristics of women at risk of initial infection and screened for superinfection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185021"], "description"=>"<p>-superinfecting variant not detected.</p>†<p>intersubtype superinfection.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "superinfection", "cases", "mombasa"], "article_id"=>784272, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_9_new_superinfection_cases_in_the_Mombasa_cohort_/784272", "title"=>"Summary of 9 new superinfection cases in the Mombasa cohort.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185019"], "description"=>"<p>Event-free survival is plotted against days at risk for 1910 women at risk for initial infection (blue) and 138 women at risk for superinfection (red).</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "superinfection"], "article_id"=>784270, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g006", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kaplan_Meier_curve_showing_initial_and_superinfection_events_over_time_at_risk_/784270", "title"=>"Kaplan-Meier curve showing initial and superinfection events over time at risk.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185016"], "description"=>"<p>Subject identifiers for the 21 cases of superinfection are listed with the 9 cases identified here listed first, followed by the 12 cases from prior studies <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Chohan2\" target=\"_blank\">[5]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Piantadosi1\" target=\"_blank\">[12]</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003593#ppat.1003593-Piantadosi2\" target=\"_blank\">[17]</a>. Time since initial infection (years) is represented as blue bars. The red rectangles represent the interval between the last timepoint at which only the initial variant was detected and the first timepoint at which the superinfecting variant was detected. The blue line marks the interval midpoint. *QB045 was HIV RNA-positive at enrollment and was therefore excluded from the incidence analysis.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology", "superinfection"], "article_id"=>784267, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_timing_of_superinfection_events_relative_to_initial_infection_events_/784267", "title"=>"Summary of timing of superinfection events relative to initial infection events.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/1185015"], "description"=>"<p><b>A.</b> Phylogenetic trees representing viral sequence from all timepoints in each genomic region analyzed. The corresponding posterior probability of monophyly is displayed. Initial variant branches are collapsed and highlighted in blue, superinfecting variant branches in red. Red branch labels mark query sequences from individual QB210 at all timepoints, black labels mark reference sequences. <b>B.</b> Maximum percent pairwise distance (PWD) between sequences within each timepoint listed or across all timepoints (All-tp). The 97.5% confidence limit of the distances observed among viral sequences within known singly infected individuals and the 2.5% confidence limit within simulated mixtures of sequences from two individuals are shown for comparison. Timepoints shown in bold type are the 3 samples originally screened; the rest were subsequently sequenced to specify superinfection timing. <sup>1</sup> PWD within 95% confidence interval observed for single infection. <sup>2</sup> PWD outside 95% confidence interval for single infection and within 95% confidence interval for dual infection. † PWD within 95% confidence intervals observed in both single and dual infection. <b>C.</b> Schematic summarizing viral variants detected in each genomic region over time (initial variant depicted in blue, superinfecting variant in red). Viral subtype is indicated.</p>", "links"=>[], "tags"=>["microbiology", "Virology", "Immunodeficiency viruses", "epidemiology"], "article_id"=>784266, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Keshet Ronen", "Connor O. McCoy", "Frederick A. Matsen", "David F. Boyd", "Sandra Emery", "Katherine Odem-Davis", "Walter Jaoko", "Kishor Mandaliya", "R. Scott McClelland", "Barbra A. Richardson", "Julie Overbaugh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003593.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Superinfection_case_QB210_/784266", "title"=>"Superinfection case QB210.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-29 06:45:56"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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Relative Metric

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