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      Temporal evolution of HIV sero-discordancy patterns among stable couples in sub-Saharan Africa

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          Abstract

          Introduction

          Objective was to examine the temporal variation of HIV sero-discordancy in select representative countries (Kenya, Lesotho, Mali, Niger, Tanzania, and Zimbabwe) in sub-Saharan Africa at different HIV epidemic scales. A sero-discordant couple is defined as a stable couple (SC) in which one partner is HIV-positive while the other is HIV-negative.

          Methods

          A deterministic compartmental mathematical model was constructed to describe HIV transmission dynamics. The model was pair-based, that is explicitly modeling formation of SCs and infection dynamics in both SCs and in single individuals. The model accommodated for different forms of infection statuses in SCs. Using population-based nationally-representative epidemiologic and demographic input data, historical (1980–2014) and future (2015–2030) trends of sero-discordancy and other demographic and epidemiologic indicators were projected throughout HIV epidemic phases.

          Results

          As the epidemics emerged, about 90% of SCs affected by HIV were sero-discordant. This proportion declined to 45%-88% at epidemic peak and stabilized as the epidemics started their natural decline. The largest reductions in sero-discordancy were in high HIV-prevalence countries. As the epidemics further declined with antiretroviral therapy (ART) scale-up, the proportion of sero-discordant couples among HIV-affected couples was projected to increase to 70%-92% by 2030. The proportion of sero-discordant couples among all SCs increased as the epidemics emerged and evolved, then peaked at 2%-20% as the epidemics peaked, and then declined as the epidemics declined to reach 0.3%-16% by 2030.

          Conclusions

          Sero-discordancy patterns varied with the evolution of the epidemics, and were affected by both epidemic phase and scale. The largest variations were found in high HIV-prevalence countries. The fraction of stable couples that are sero-discordant, as opposed to being sero-concordant positive, was projected to increase with ART scale-up and further HIV incidence decline over the coming two decades. These findings inform strategic planning and resource allocation for interventions among sero-discordant couples.

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          Most cited references21

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          New heterosexually transmitted HIV infections in married or cohabiting couples in urban Zambia and Rwanda: an analysis of survey and clinical data.

          Sub-Saharan Africa has a high rate of HIV infection, most of which is attributable to heterosexual transmission. Few attempts have been made to assess the extent of HIV transmission within marriages, and HIV-prevention efforts remain focused on abstinence and non-marital sex. We aimed to estimate the proportion of heterosexual transmission of HIV which occurs within married or cohabiting couples in urban Zambia and Rwanda each year. We used population-based data from Demographic and Health Surveys (DHS) on heterosexual behaviour in Zambia in 2001-02 and in Rwanda in 2005. We also used data on the HIV serostatus of married or cohabiting couples and non-cohabiting couples that was collected through a voluntary counselling and testing service for urban couples in Lusaka, in Zambia, and Kigali, in Rwanda. We estimated the probability that an individual would acquire an incident HIV infection from a cohabiting or non-cohabiting sexual partner, and then the proportion of total heterosexual HIV transmission which occurs within married or cohabiting couples in these settings each year. We analysed DHS data from 1739 Zambian women, 540 Zambian men, 1176 Rwandan women, and 606 Rwandan men. Under our base model, we estimated that 55.1% to 92.7% of new heterosexually acquired HIV infections among adults in urban Zambia and Rwanda occurred within serodiscordant marital or cohabiting relationships, depending on the sex of the index partner and on location. Under our extended model, which incorporated the higher rates of reported condom use that we found with non-cohabiting partners, we estimated that 60.3% to 94.2% of new heterosexually acquired infections occurred within marriage or cohabitation. We estimated that an intervention for couples which reduced transmission in serodiscordant urban cohabiting couples from 20% to 7% every year could avert 35.7% to 60.3% of heterosexually transmitted HIV infections that would otherwise occur. Since most heterosexual HIV transmission for both men and women in urban Zambia and Rwanda takes place within marriage or cohabitation, voluntary counselling and testing for couples should be promoted, as should other evidence-based interventions that target heterosexual couples.
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            Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa.

            Mounting evidence has revealed pathological interactions between HIV and malaria in dually infected patients, but the public health implications of the interplay have remained unclear. A transient almost one-log elevation in HIV viral load occurs during febrile malaria episodes; in addition, susceptibility to malaria is enhanced in HIV-infected patients. A mathematical model applied to a setting in Kenya with an adult population of roughly 200,000 estimated that, since 1980, the disease interaction may have been responsible for 8,500 excess HIV infections and 980,000 excess malaria episodes. Co-infection might also have facilitated the geographic expansion of malaria in areas where HIV prevalence is high. Hence, transient and repeated increases in HIV viral load resulting from recurrent co-infection with malaria may be an important factor in promoting the spread of HIV in sub-Saharan Africa.
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              Regional Differences in Prevalence of HIV-1 Discordance in Africa and Enrollment of HIV-1 Discordant Couples into an HIV-1 Prevention Trial

              Background Most HIV-1 transmission in Africa occurs among HIV-1-discordant couples (one partner HIV-1 infected and one uninfected) who are unaware of their discordant HIV-1 serostatus. Given the high HIV-1 incidence among HIV-1 discordant couples and to assess efficacy of interventions for reducing HIV-1 transmission, HIV-1 discordant couples represent a critical target population for HIV-1 prevention interventions and prevention trials. Substantial regional differences exist in HIV-1 prevalence in Africa, but regional differences in HIV-1 discordance among African couples, has not previously been reported. Methodology/Principal Findings The Partners in Prevention HSV-2/HIV-1 Transmission Trial (“Partners HSV-2 Study”), the first large HIV-1 prevention trial in Africa involving HIV-1 discordant couples, completed enrollment in May 2007. Partners HSV-2 Study recruitment data from 12 sites from East and Southern Africa were used to assess HIV-1 discordance among couples accessing couples HIV-1 counseling and testing, and to correlate with enrollment of HIV-1 discordant couples. HIV-1 discordance at Partners HSV-2 Study sites ranged from 8–31% of couples tested from the community. Across all study sites and, among all couples with one HIV-1 infected partner, almost half (49%) of couples were HIV-1 discordant. Site-specific monthly enrollment of HIV-1 discordant couples into the clinical trial was not directly associated with prevalence of HIV-1 discordance, but was modestly correlated with national HIV-1 counseling and testing rates and access to palliative care/basic health care (r = 0.74, p = 0.09). Conclusions/Significance HIV-1 discordant couples are a critical target for HIV-1 prevention in Africa. In addition to community prevalence of HIV-1 discordance, national infrastructure for HIV-1 testing and healthcare delivery and effective community outreach strategies impact recruitment of HIV-1 discordant couples into HIV-1 prevention trials.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Project administrationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 April 2018
                2018
                : 13
                : 4
                : e0196613
                Affiliations
                [1 ] Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation - Education City, Doha, Qatar
                [2 ] Population Health Research Institute, St George’s, University of London, London, United Kingdom
                [3 ] Department of Healthcare Policy and Research, Weill Cornell Medicine, Cornell University, New York, New York, United States of America
                The Ohio State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0790-0506
                Article
                PONE-D-17-41604
                10.1371/journal.pone.0196613
                5927442
                29708995
                441de465-1a7d-4ffd-880a-e912da3bf4e8
                © 2018 Awad et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 November 2017
                : 15 April 2018
                Page count
                Figures: 4, Tables: 1, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100008982, Qatar National Research Fund;
                Award ID: 6-681-3-173
                Award Recipient :
                This publication was made possible by NPRP grant number 6-681-3-173 from the Qatar National Research Fund (a member of Qatar Foundation). The findings achieved herein are solely the responsibility of the authors.
                Categories
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                Medicine and health sciences
                Epidemiology
                HIV epidemiology
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                Medical Microbiology
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                Immunodeficiency Viruses
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