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. 2016 Dec 7;11(12):e0166805.
doi: 10.1371/journal.pone.0166805. eCollection 2016.

Male Circumcision and the Epidemic Emergence of HIV-2 in West Africa

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Male Circumcision and the Epidemic Emergence of HIV-2 in West Africa

João Dinis Sousa et al. PLoS One. .

Abstract

Background: Epidemic HIV-2 (groups A and B) emerged in humans circa 1930-40. Its closest ancestors are SIVsmm infecting sooty mangabeys from southwestern Côte d'Ivoire. The earliest large-scale serological surveys of HIV-2 in West Africa (1985-91) show a patchy spread. Côte d'Ivoire and Guinea-Bissau had the highest prevalence rates by then, and phylogeographical analysis suggests they were the earliest epicenters. Wars and parenteral transmission have been hypothesized to have promoted HIV-2 spread. Male circumcision (MC) is known to correlate negatively with HIV-1 prevalence in Africa, but studies examining this issue for HIV-2 are lacking.

Methods: We reviewed published HIV-2 serosurveys for 30 cities of all West African countries and obtained credible estimates of real prevalence through Bayesian estimation. We estimated past MC rates of 218 West African ethnic groups, based on ethnographic literature and fieldwork. We collected demographic tables specifying the ethnic partition in cities. Uncertainty was incorporated by defining plausible ranges of parameters (e.g. timing of introduction, proportion circumcised). We generated 1,000 sets of past MC rates per city using Latin Hypercube Sampling with different parameter combinations, and explored the correlation between HIV-2 prevalence and estimated MC rate (both logit-transformed) in the 1,000 replicates.

Results and conclusions: Our survey reveals that, in the early 20th century, MC was far less common and geographically more variable than nowadays. HIV-2 prevalence in 1985-91 and MC rates in 1950 were negatively correlated (Spearman rho = -0.546, IQR: -0.553--0.546, p≤0.0021). Guinea-Bissau and Côte d'Ivoire cities had markedly lower MC rates. In addition, MC was uncommon in rural southwestern Côte d'Ivoire in 1930.The differential HIV-2 spread in West Africa correlates with different historical MC rates. We suggest HIV-2 only formed early substantial foci in cities with substantial uncircumcised populations. Lack of MC in rural areas exposed to bushmeat may have had a role in successful HIV-2 emergence.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. HIV-2 seroprevalence in adults without specific risk factors in West Africa, 1985–91.
Complete information on HIV-2 prevalence rates is in S1 Dataset. The checkered area indicates the historical (pre-1950) range of sooty mangabeys [–53].
Fig 2
Fig 2. Estimated MC frequencies for the West African cities.
Estimated MC frequencies in 1950 (A) and 1988 (B) for the West African cities. Boxes indicate the interquartile range (IQR) of the frequencies; median is indicated by a horizontal line within the box, and whiskers extend to the farthest values that are not more than 1.5 times the IQR away from the box. Cities of the same country appear with the same color. Country colors: Côte d'Ivoire, red; Liberia, dark green; Sierra Leone, green; Guinea, dark cyan; Guinea-Bissau, magenta; Senegal, brown; Gambia, gray; Cape Verde, dark gray; Mauritania, yellow; Mali, chocolate; Burkina Faso, tomato; Ghana, violet-red; Togo, blue; Benin, dodger blue; Nigeria, deep sky blue; Niger, light gray.
Fig 3
Fig 3. The estimated MC frequencies in 8 large cities at or near the sooty mangabey range in 1930.
Cities of the same country appear with the same color. The country colors are the same as in Fig 2 (see Fig 2 legend).
Fig 4
Fig 4. The spread of MC practices at or near the sooty mangabey range in early 20th century.
The information supporting this map is in S2 Dataset, with additional explanations in S1 Text. The checkered area indicates the historical (pre-1950) range of sooty mangabeys [–53].

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Grants and funding

The research done by JDS and AMV in this study has been supported in part by grant G.0611.09N, funded by the Fonds voor Wetenschappelijk Onderzoek – Flanders (FWO, http://www.fwo.be/en/), Belgium. MPT’s fieldwork in Guinea-Bissau was conducted within the framework of the project “The prophetess and the rice farmer: innovations in religion, agriculture and gender in Guinea-Bissau”, PTDC/AFR/111546/2009, funded by Fundação para a Ciência e Tecnologia, (FCT, http://www.fct.pt/), Portugal. VM is a Fellow of the Parmenides Center for the Conceptual Foundations of Science, part of Parmenides Foundation (https://www.parmenides-foundation.org/home/), Germany. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.