Can Prenatal Malaria Exposure Produce an Immune Tolerant Phenotype?: A Prospective Birth Cohort Study in Kenya
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{"title"=>"Can prenatal malaria exposure produce an immune tolerant phenotype?: A prospective birth cohort study in Kenya", "type"=>"journal", "authors"=>[{"first_name"=>"Indu", "last_name"=>"Malhotra", "scopus_author_id"=>"6603041371"}, {"first_name"=>"Arlene", "last_name"=>"Dent", "scopus_author_id"=>"8706028700"}, {"first_name"=>"Peter", "last_name"=>"Mungai", "scopus_author_id"=>"6603339309"}, {"first_name"=>"Alex", "last_name"=>"Wamachi", "scopus_author_id"=>"6602463113"}, {"first_name"=>"John H.", "last_name"=>"Ouma", "scopus_author_id"=>"7004521768"}, {"first_name"=>"David L.", "last_name"=>"Narum", "scopus_author_id"=>"6603994338"}, {"first_name"=>"Eric", "last_name"=>"Muchiri", "scopus_author_id"=>"6602001513"}, {"first_name"=>"Daniel J.", "last_name"=>"Tisch", "scopus_author_id"=>"6507774421"}, {"first_name"=>"Christopher L.", "last_name"=>"King", "scopus_author_id"=>"7401525894"}], "year"=>2009, "source"=>"PLoS Medicine", "identifiers"=>{"scopus"=>"2-s2.0-68049144807", "sgr"=>"68049144807", "issn"=>"15491277", "doi"=>"10.1371/journal.pmed.1000116", "pmid"=>"19636353", "isbn"=>"1549-1676 (Electronic)", "pui"=>"355033311"}, "id"=>"b0eeaff0-f59d-308a-b834-3240444fa5ba", "abstract"=>"BACKGROUND: Malaria in pregnancy can expose the fetus to malaria-infected erythrocytes or their soluble products, thereby stimulating T and B cell immune responses to malaria blood stage antigens. We hypothesized that fetal immune priming, or malaria exposure in the absence of priming (putative tolerance), affects the child's susceptibility to subsequent malaria infections. METHODS AND FINDINGS: We conducted a prospective birth cohort study of 586 newborns residing in a malaria-holoendemic area of Kenya who were examined biannually to age 3 years for malaria infection, and whose malaria-specific cellular and humoral immune responses were assessed. Newborns were classified as (i) sensitized (and thus exposed), as demonstrated by IFNgamma, IL-2, IL-13, and/or IL-5 production by cord blood mononuclear cells (CBMCs) to malaria blood stage antigens, indicative of in utero priming (n = 246), (ii) exposed not sensitized (mother Plasmodium falciparum [Pf]+ and no CBMC production of IFNgamma, IL-2, IL-13, and/or IL-5, n = 120), or (iii) not exposed (mother Pf-, no CBMC reactivity, n = 220). Exposed not sensitized children had evidence for prenatal immune experience demonstrated by increased IL-10 production and partial reversal of malaria antigen-specific hyporesponsiveness with IL-2+IL-15, indicative of immune tolerance. Relative risk data showed that the putatively tolerant children had a 1.61 (95% confidence interval [CI] 1.10-2.43; p = 0.024) and 1.34 (95% CI 0.95-1.87; p = 0.097) greater risk for malaria infection based on light microscopy (LM) or PCR diagnosis, respectively, compared to the not-exposed group, and a 1.41 (95%CI 0.97-2.07, p = 0.074) and 1.39 (95%CI 0.99-2.07, p = 0.053) greater risk of infection based on LM or PCR diagnosis, respectively, compared to the sensitized group. Putatively tolerant children had an average of 0.5 g/dl lower hemoglobin levels (p = 0.01) compared to the other two groups. Exposed not sensitized children also had 2- to 3-fold lower frequency of malaria antigen-driven IFNgamma and/or IL-2 production (p<0.001) and higher IL-10 release (p<0.001) at 6-month follow-ups, when compared to sensitized and not-exposed children. Malaria blood stage-specific IgG antibody levels were similar among the three groups. CONCLUSIONS: These results show that a subset of children exposed to malaria in utero acquire a tolerant phenotype to blood-stage antigens that persists into childhood and is associated with an increased susceptibility to malaria infection and anemia. This finding could have important implications for malaria vaccination of children residing in endemic areas.", "link"=>"http://www.mendeley.com/research/prenatal-malaria-exposure-produce-immune-tolerant-phenotype-prospective-birth-cohort-study-kenya", "reader_count"=>109, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>26, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>5, "Student > Master"=>20, "Other"=>5, "Student > Bachelor"=>3, "Lecturer"=>2, "Professor"=>5}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>26, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>5, "Student > Master"=>20, "Other"=>5, "Student > Bachelor"=>3, "Lecturer"=>2, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Engineering"=>1, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>51, "Medicine and Dentistry"=>31, "Neuroscience"=>1, "Psychology"=>1, "Social Sciences"=>4, "Immunology and Microbiology"=>8, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>31}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>4}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>8}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>51}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>2}}, "reader_count_by_country"=>{"Afghanistan"=>1, "Burkina Faso"=>1, "Belgium"=>1, "United States"=>3, "Brazil"=>1, "United Kingdom"=>3, "Malaysia"=>1, "Thailand"=>1, "Spain"=>1, "Indonesia"=>1, "India"=>2}, "group_count"=>2}

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  • {"files"=>["https://ndownloader.figshare.com/files/890229"], "description"=>"<p>There were no differences between the proportion of children with antibody responses to MSP1<sub>42</sub> and AMA1 between the three groups beginning at 12 months of age as determined by a generalized estimating equation described in <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#pmed-1000116-g005\" target=\"_blank\">Figure 5</a> (exposed not sensitized group compared to exposed sensitized group: relative risk for MSP1<sub>42</sub>, 1.05 [0.88–1.17], <i>p</i> = 0.457; for AMA1, 0.87 [0.74–1.11], <i>p</i> = 0.251), but a significant reduction for EBA-175–specific IgG, 0.41 [0.28–0.97], <i>p</i> = 0.03. Similar effect sizes were observed for exposed not sensitized children compared to not exposed children (unpublished data).</p>", "links"=>[], "tags"=>["prenatal", "malaria", "eba-175", "igg", "responses"], "article_id"=>560670, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_association_of_prenatal_exposure_to_malaria_with_acquisition_of_MSP1_42_and_AMA1_and_EBA_175_specific_IgG_responses_in_all_children_/560670", "title"=>"The association of prenatal exposure to malaria with acquisition of MSP1<sub>42</sub> and AMA1, and EBA-175 specific IgG responses in all children.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:13:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/890362"], "description"=>"a<p>Values indicate the population mean of the ratio of a positive result to total observations for each individual. The average number of observations for each group is shown in <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#pmed-1000116-g001\" target=\"_blank\">Figure 1</a>.</p>b<p>Generalized estimating equation adjusted for location, time, and repeated measures as described more fully in the <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#s2\" target=\"_blank\">Methods</a> section.</p>", "links"=>[], "tags"=>["prenatal", "susceptibility"], "article_id"=>560814, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.t002", "stats"=>{"downloads"=>0, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_of_prenatal_immune_experience_with_susceptibility_to_P_falciparum_infection_in_early_childhood_/560814", "title"=>"Association of prenatal immune experience with susceptibility to <i>P. falciparum</i> infection in early childhood.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 05:14:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/890059"], "description"=>"<p>(A) Exposed not sensitized children have a lower frequency of IFNγ and IL-2 production, and/or lymphocyte proliferation by PBMCs (a positive response is defined in the text and <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#s2\" target=\"_blank\">method</a> section) compared to exposed sensitized children and not-exposed children using a generalized estimating equations that adjusts for time, location, and repeated measures as more fully described in the <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#s2\" target=\"_blank\">Methods</a> section (relative risk, [95% confidence interval], exposed not sensitized children compared to exposed sensitized children: 0.28 [0.15–0.37], <i>p</i> = 0.0003 for MSP1; 0.33 [0.20–0.51], <i>p</i> = 0.0008 for PfP0; 0.36 [0.19–0.74], <i>p</i> = 0.005 for EBA175; and 1.07 [0.89–1.65] for tetanus toxoid). Similar effect sizes were observed for exposed not sensitized children compared to not exposed children (unpublished data). (B) The frequency of antigen-driven IL-10 is higher in the exposed not sensitized children than in exposed sensitized (relative risk for MSP1, 1.67 [1.35–2.73], <i>p</i> = 0.0007; for PfP0 1.45 [1.03–2.51], <i>p</i> = 0.02; for EBA175 1.38 [0.99–2.42], <i>p</i> = 0.05; and for tetanus toxoid 1.04 [0.85–1.12], <i>p</i> = 0.73. (C) The frequency of malaria antigen-induced IL-5 and/or IL-13 cytokine responses are equivalent for the three groups (relative risk for exposed not sensitized compared to exposed sensitized children: for MSP1, 0.97 [0.79–1.21], <i>p</i> = 0.35; for PfP0 0.92 [0.73–1.36], <i>p</i> = 0.47; for EBA175, 0.83 [0.64–1.09], <i>p</i> = 0.16; and for tetanus toxoid, 1.01 [0.93–1.06], <i>p</i> = 0.61. Similar effect sizes were observed for exposed not sensitized children compared to not exposed children (unpublished data).</p>", "links"=>[], "tags"=>["prenatal", "malaria", "antigen", "tetanus", "toxoid-driven", "cytokine", "biannually", "36", "months"], "article_id"=>560495, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_association_of_prenatal_malaria_exposure_with_the_frequency_of_malaria_antigen_and_tetanus_toxoid_driven_cytokine_production_measured_biannually_to_36_months_of_age_/560495", "title"=>"The association of prenatal malaria exposure with the frequency of malaria antigen and tetanus toxoid-driven cytokine production measured biannually to 36 months of age.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:12:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/889726"], "description"=>"<p>Median malaria antigen-driven IL-10 production for all subjects in the three experimental groups.</p>", "links"=>[], "tags"=>["malaria", "antigen-driven", "il-10", "subjects"], "article_id"=>560174, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Median_malaria_antigen_driven_IL_10_production_for_all_subjects_in_the_three_experimental_groups_/560174", "title"=>"Median malaria antigen-driven IL-10 production for all subjects in the three experimental groups.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:11:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/890320"], "description"=>"a<p>Maternal/newborn Pf infection was assessed by either LM and/or RTQPCR detection of parasites in maternal, cord, and/or intervillous placental blood.</p>b<p>Forty-three of the individuals in this group had T cell responses, but without maternal/newborn malaria infection at delivery.</p>c<p><i>p</i>-Value of exposed not sensitized compared to exposed sensitized group.</p>d<p><i>p</i>-Value of exposed not sensitized compared to not exposed group.</p>", "links"=>[], "tags"=>["characteristics", "pairs", "newborn", "malaria", "responses"], "article_id"=>560760, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.t001", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Demographic_characteristics_of_maternal_8211_fetal_pairs_according_to_newborn_malaria_exposure_status_and_cord_blood_T_cell_responses_to_MSP1_PfP0_and_EBA_175_/560760", "title"=>"Demographic characteristics of maternal–fetal pairs according to newborn malaria exposure status and cord blood T cell responses to MSP1, PfP0, and EBA-175.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 05:14:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/889898"], "description"=>"<p>The overall mean hemoglobin levels in exposed not sensitized (putatively tolerant) children were significantly lower than the exposed sensitized (<i>p</i> = 0.03) and not exposed children (<i>p</i> = 0.01) based on a repeated measures model (described in <a href=\"http://www.plosmedicine.org/article/info:doi/10.1371/journal.pmed.1000116#pmed-1000116-t002\" target=\"_blank\">Table 2</a>). Analysis was adjusted for children's height and weight (BMI) and helminth coinfection.</p>", "links"=>[], "tags"=>["sensitized", "children", "reduced", "hemoglobin", "levels", "36", "months"], "article_id"=>560339, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Exposed_not_sensitized_children_at_birth_show_reduced_mean_hemoglobin_levels_throughout_36_months_of_follow_up_/560339", "title"=>"Exposed not sensitized children at birth show reduced mean hemoglobin levels throughout 36 months of follow-up.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:12:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/889820"], "description"=>"<p>Values shown are the fold-increase in cpm in cultures with IL-2+IL-15+malaria antigens divided by cultures with IL-2+IL-15 alone. A positive response was considered >2-fold increase (dashed horizontal line). Statistical differences were calculated by Chi-square comparing the proportion of positive responders. Solid horizontal bars indicate median values.</p>", "links"=>[], "tags"=>["malaria-antigen", "driven", "lymphocyte", "proliferation", "cbmcs", "subset", "exposed", "sensitized", "newborns"], "article_id"=>560260, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g003", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Augmentation_of_malaria_antigen_driven_lymphocyte_proliferation_by_CBMCs_in_a_subset_of_exposed_sensitized_n_21_exposed_not_sensitized_n_21_and_not_exposed_n_19_newborns_in_the_presence_of_IL_2_IL_15_/560260", "title"=>"Augmentation of malaria-antigen driven lymphocyte proliferation by CBMCs in a subset of exposed sensitized (<i>n</i> = 21), exposed not sensitized (<i>n</i> = 21), and not exposed (<i>n</i> = 19) newborns in the presence of IL-2+IL-15.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:11:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/889624"], "description"=>"<p>Flow diagram of birth cohort study.</p>", "links"=>[], "tags"=>["diagram", "cohort"], "article_id"=>560065, "categories"=>["Immunology", "Infectious Diseases", "Physics", "Medicine"], "users"=>["Indu Malhotra", "Arlene Dent", "Peter Mungai", "Alex Wamachi", "John H. Ouma", "David L. Narum", "Eric Muchiri", "Daniel J. Tisch", "Christopher L. King"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.1000116.g001", "stats"=>{"downloads"=>3, "page_views"=>38, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Flow_diagram_of_birth_cohort_study_/560065", "title"=>"Flow diagram of birth cohort study.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:10:37"}

PMC Usage Stats | Further Information

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  • {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"4", "full-text"=>"31", "year"=>"2012", "pdf"=>"11", "unique-ip"=>"29", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
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  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
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  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
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Relative Metric

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