Penile viral shedding results by weekly intervals from the day of circumcision to 6 weeks postsurgery are presented for 29 ART-naive men (Fig. 2). Five (17.2%) of the 29 men had detectable viral shedding from the penis before circumcision and 80% of these (4/5) had CD4+ T-cell counts <350 cells per cubic millimeter but were not yet on ART. Three of the 29 men who had no detectable viral shedding at baseline had no measurable virus at any time postcircumcision. The remaining 26 men had an upsurge in penile viral shedding which peaked at 1 week postcircumcision then declined to undetectable levels within 6 weeks in all but 1 individual, whose viral shedding became undetectable at week 7 (not shown in Fig. 2). Multivariate analysis of variance from baseline to 6 weeks showed highly significant changes in viral shedding after circumcision (Table 2).
The temporal sequence of clinical certification of wound healing, self-reported resumption of sex, and change in penile HIV viral shedding is shown in Figure 3. Viral shedding peaked at weeks 1 and 2 before any of the men resumed sex. Weeks 3–5 were characterized by a steep decline in viral shedding and increases in the proportion of men certified as healed or resuming sex. By week 6, 45% of men had resumed sex and 93% of men were certified as fully healed. Most importantly, in 96.6% (28/29) of the men, no viral shedding was detected after certification of wound healing. Only 1 man (3.4%) still had penile viral shedding from an unhealed wound when he first resumed sex, and he reported using a condom. Neither the mean viral load nor the proportion of men shedding virus differed between those who resumed sex early compared with those who delayed sex to 6 weeks.
There is concern that widespread MC programs for HIV prevention could increase the risk of HIV transmission from seropositive men to their sexual partners if the surgical procedure and subsequent wound healing processes result in elevated plasma viral loads and increases in penile viral shedding.4,25 We found no change in CD4+ T-cell count from baseline to 2 weeks postcircumcision in seropositive men who were on ART and a slight increase among ART-naive men from 417 to 456 cells per cubic millimeter. We found no increase in plasma viral load at any point during 6 weeks after circumcision, a finding that differs from a previous study by Wawer at al4 in Rakai, Uganda, where plasma viral loads among ART-naive men were elevated above baseline, 4 weeks after circumcision, by a mean of 0.20 log10 copies per milliliter. Although our sample size of 19 men was small, limiting power to detect significant changes, the viral loads of men in our study did not rise, but rather declined, albeit insignificantly, after circumcision from a mean of 4.86 log10 copies per milliliter at baseline to 4.65 log10 copies per milliliter at week 4 postsurgery. It is difficult to determine the reasons for the differences between our results and those from Rakai. The Rakai sample was restricted to men who had CD4+ T-cell counts >350 cells per cubic millimeter and to those with detectable virus at baseline. Their baseline levels of plasma virus (mean 4.30 log10 copies/mL) were somewhat less than those of the men in our study. If we restrict our analysis to the 10 men whose CD4+ T-cell counts were >350 per cubic millimeter and virus at baseline was detectable, we still observe a mean viral load of 4.68 log10 copies per milliliter at baseline with a slight reduction to 4.62 log10 copies per milliliter at week 4 postsurgery.
Our finding that penile viral shedding returns essentially to baseline levels by week 6 postsurgery should be considered as welcome in view of the WHO guidelines recommending 42 days of sexual abstinence after medical circumcision.9 We have previously shown that 94% of men are fully healed by week 6 postsurgery, and that, although approximately 38% of men resume sex before 42 days postcircumcision, only 7% had unprotected sex before they were certified as fully healed.20,21 Wawer et al4 noted that the risk of HIV transmission because of sex before the circumcision wound is healed is brief and likely to be small in proportion to the number of new infections to be averted in the population over decades through the protective effect of MC. Our results not only support this view but also suggest that the risks of HIV transmission to the partners of HIV-positive men are considerably less than previously considered.4,30 Nevertheless, we have shown that 24% of ART-naive HIV-positive men continue shedding virus above baseline up to 4 weeks postsurgery; thus developing effective counseling and communications strategies for both men and their female partners to avoid sex before 42 days after circumcision and to optimize condom use remains an essential component of a comprehensive MC program for HIV prevention.9,20
Our study has a number of limitations. The men recruited for the study, although residents of Kisumu who were seeking MC, may not be representative of the full range of HIV-positive men in the community who could be served by the Kenyan MC program. All the study men accepted HIV testing; in the Kenya MC program 92% of men agree to be tested before circumcision. Because men in this study were counseled weekly, the participants may have been more motivated to properly care for their wound or to refrain from sex than those circumcised as part of the national MC program. Consequently, the timing and rate of unprotected sex reported here may be different from routine MC program settings, although the proportion of men we found resuming sex before 42 days postcircumcision is very similar to findings from 2 previous studies conducted among clients attending the Kenya MC program.31,32 Our sample size, especially for plasma viral load, is small, limiting our power to detect significant changes over time. However, the changes that we observed were very small and, if anything, were downward. The data are sufficient to conclude that plasma viral load did not increase from before to after circumcision in these men in Kisumu. A further limitation is that we do not know if circumcision surgery causes increases in HIV in the ejaculate. It is not feasible to collect semen samples from study participants by asking them to masturbate with an open wound. Recently, postprostatic massage was shown to be a feasible and valid method for assessing male genitourinary tract HIV shedding, but this was not attempted in this study.33
The authors are grateful to Drs Godfrey Kigozi, Stephen Watya, and the Rakai Health Sciences Program for generously sharing their protocol.
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