Extra-couple HIV transmission in sub-Saharan Africa: a mathematical modelling study of survey data

Abstract

Background: The proportion of heterosexual HIV transmission in sub-Saharan Africa that occurs within cohabiting partnerships, compared with that in single people or extra-couple relationships, is widely debated. We estimated the proportional contribution of different routes of transmission to new HIV infections. As plans to use antiretroviral drugs as a strategy for population-level prevention progress, understanding the importance of different transmission routes is crucial to target intervention efforts.

Methods: We built a mechanistic model of HIV transmission with data from Demographic and Health Surveys (DHS) for 2003-2011, of 27,201 cohabiting couples (men aged 15-59 years and women aged 15-49 years) from 18 sub-Saharan African countries with information about relationship duration, age at sexual debut, and HIV serostatus. We combined this model with estimates of HIV survival times and country-specific estimates of HIV prevalence and coverage of antiretroviral therapy (ART). We then estimated the proportion of recorded infections in surveyed cohabiting couples that occurred before couple formation, between couple members, and because of extra-couple intercourse.

Findings: In surveyed couples, we estimated that extra-couple transmission accounted for 27-61% of all HIV infections in men and 21-51% of all those in women, with ranges showing intercountry variation. We estimated that in 2011, extra-couple transmission accounted for 32-65% of new incident HIV infections in men in cohabiting couples, and 10-47% of new infections in women in such couples. Our findings suggest that transmission within couples occurs largely from men to women; however, the latter sex have a very high-risk period before couple formation.

Interpretation: Because of the large contribution of extra-couple transmission to new HIV infections, interventions for HIV prevention should target the general sexually active population and not only serodiscordant couples.

Funding: US National Institutes of Health, US National Science Foundation, and J S McDonnell Foundation.

Figure 1. Schematic diagram of the couple transmission model

This diagram illustrates how the model relates the infection process to a couple’s relationship and sexual histories for an example Zambian couple. Each partner (represented by the black lines) can be infected prior to couple formation (gray arrows) beginning from the month of their sexual debut (t_msd or t_fsd for males and females, respectively) until the month the couple is formed (t_cf). From couple formation until the month prior to their DHS interview (t_int), an individual can be infected by their partner if their partner is positive (blue arrows), or from extra-couple intercourse (red arrows). For each month of an individual’s sexual activity, the hazard of infection is the product of a gender-route-specific transmission coefficient (i.e., one parameter for each arrow) and the probability intercourse is with an infectious individual. The probability intercourse is with an infectious individual is determined by the probability the partner is HIV positive for within-couple transmission, and estimated as the opposite gender’s population infectious HIV prevalence for before-partnership or extra-couple transmission. We assume individuals on ART are not infectious and calculate infectious HIV prevalence as (HIV prevalence)×(1 − ART coverage). Thus, the difference between the solid and dashed lines is ART coverage. For this example couple, the gray (respectively, red) areas under the prevalence curves represent the infectious HIV prevalence in the opposing gender that the partners would be mixing with during before-couple (extra-couple) intercourse.

Figure 2. Model fit to Zambia couples DHS data

Each point in this figure represents a couple. Couples are divided between panels based on their serostatus: male positive discordant (A), female positive discordant (C), and concordant positive (B, D). Points are plotted as a function of the date of couple formation and the number of years the male (A, B) or female (C,D) was sexual active before the couple formed. Blue lines give the population prevalence of HIV, excluding the proportion on antiretroviral treatment (and thus not infectious), in the opposite gender (i.e., from whom before-partnership or extra-couple transmission occurs). The color of each point represents the median fitted posterior probability that a seropositive male (A, B) or female (C, D) was infected from extra-couple transmission rather than before couple formation for serodiscordant couples and, for concordant positive couples, transmission from a positive partner. For serodiscordant couples (A, C), the probability that transmission occurred extra-couply is greater for seropositive individuals who had shorter durations of sexual activity prior to couple formation, or whose couple formation occurred earlier on in the epidemic or long enough ago such that they would have been unlikely to survive to DHS sampling if infected prior to couple formation. The same patterns hold for concordant positive couples (B, D), though the probability of extra-couple transmission is reduced because within-partner transmission is also possible.

Figure 3. Estimated proportion of transmission from each route of transmission by gender, country, and couple serostatus for couples interviewed in the DHS

This figure shows the estimated proportional contribution of HIV transmission from intercourse before the formation of the current partnership (gray), from extra-couple intercourse during the current partnership (red), and from intercourse with the current partner (blue). Panels show results by couple serostatus and gender. Bars give posterior median estimates (values and 95% credible intervals are given in Table S7). These estimates only reflect the estimated contribution of each transmission route amongst observed couples, and do not account for survival bias due to couples that could not be surveyed because one or more partner died before the DHS sampling (see Table S8).

Figure 4. Projected proportion of incidence over the next year in cohabiting couples that will be due to extra-couple intercourse by country

This figure shows the estimated proportion of projected incidence that will be caused by extra-couple transmission over the next year in all males and females testing seronegative (i.e., either gender in concordant negative couples, males in female-positive serodiscordant couples, and females in male-positive serodiscordant couples) during DHS sampling. Negative individuals in discordant couples can be infected either by extra-couple transmission or by their HIV positive partner. Negative individuals in concordant negative couples can be infected either by extra-couple transmission or by their partner if their partner becomes infected by extra-couple transmission in the next year. Values and 95% credible intervals are reported in Table S10.