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Changes in Plasma Viral Load and Penile Viral Shedding After Circumcision Among HIV-Positive Men in Kisumu, Kenya

Odoyo-June, Elijah MBCHB, MSc*,†; Rogers, John H. BS, MPH; Jaoko, Walter MBCHB, PhD*,†; Bailey, Robert C. PhD, MPH*,‡

JAIDS Journal of Acquired Immune Deficiency Syndromes: December 15th, 2013 - Volume 64 - Issue 5 - p 511–517
doi: 10.1097/QAI.0b013e3182a7ef05
Epidemiology and Prevention

Background: We conducted a prospective cohort study of HIV-positive men aged 18–35 years in Kisumu, Kenya to determine if medical circumcision of ART-naive HIV-positive men leads to increased viral load and penile viral shedding.

Methods: From 108 HIV-positive men circumcised by forceps-guided method and followed up weekly for 6 weeks, 29 men were evaluated for penile viral shedding. HIV-1 RNA was measured in plasma from 19 men and in penile lavage samples from 29 men. Samples were collected before circumcision and at weekly intervals for 6 weeks or until the circumcision wound was healed. CD4+ T-cell counts from 102 HIV-positive men were determined at baseline and at 2 weeks thereafter. Wounds with healthy scar, no scab or opening, and no suture tracks were deemed healed.

Results: Among 65 ART-naive men, mean CD4+ T-cell count increased from 417 cells per cubic millimeter at baseline to 456 cells per cubic millimeter after 2 weeks (P = 0.04), but did not change in the 37 men on ART (P = 0.81). There was no change in HIV plasma viral load (P = 0.36), but penile viral shedding rose significantly within 1 week after circumcision then declined to undetectable levels by 6 weeks (multivariate analysis of variance; P < 0.001). In 28 of 29 men (96.6%), there was no detectable viral shedding after certification of wound healing.

Conclusions: Medical circumcision among ART-naive HIV-infected men results in a transitory rise in penile viral shedding before complete wound healing, which should pose no additional risk of HIV transmission if men adhere to 6 weeks postcircumcision sexual abstinence and use condoms consistently.

*Nyanza Reproductive Health Society, Kisumu, Kenya;

University of Nairobi, Nairobi, Kenya; and

Division of Epidemiology and Biostatistics University of Illinois at Chicago, Illinois.

Correspondence to: Elijah Odoyo-June, MBCHB, MSc, Nyanza Reproductive Health Society, P.O. Box 1764, Kisumu 40100, Kenya (e-mail:

Supported by the University of Illinois at Chicago through a grant from the Bill and Melinda Gates Foundation to FHI360. R.C.B. was supported in part by the Chicago Developmental Center for AIDS Research (D-CFAR), an National Institutes of Health (NIH) funded program (P30 AI 082151). Clement Zeh, Julie Okonji, Edith Nyagaya, Lawrence Agunda, and Ruth Murugu provided technical laboratory support for this work.

E.O.J. designed the study, collected data, and performed data analysis, interpretation, and writing. R.C.B designed the study and performed data analysis, interpretation, and writing. J.H.R. designed the study, performed data analysis, interpretation, and writing. W.J. performed analysis, interpretation, critical review, and writing. Clement Zeh, Julie Okonji, Edith Nyagaya, Lawrence Agunda, and Ruth Murugu provided technical laboratory support for this work.

The authors have no conflicts of interest to disclose.

Received April 09, 2013

Accepted July 23, 2013

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Voluntary medical male circumcision (MC) is a proven intervention for reducing HIV incidence in heterosexual men.1–3 However, widespread circumcision of HIV-positive men may mitigate the public health benefits of MC. HIV-positive men may have increased viral shedding after circumcision, thereby exposing their sex partners to higher risk of HIV infection.4 In the ongoing scale-up of MC, many HIV-infected men are likely to be circumcised without knowledge of their HIV status or if they choose circumcision for non-HIV prevention benefits such as improved hygiene, reduced risk of phimosis, paraphimosis, genital ulcer disease, HSV-2, and HPV.5–7 Although the HIV testing rate among men seeking MC in Kenya is approximately 92%,8 not all programs may be as successful; HIV-positive men will inevitably be circumcised with an unknown HIV status. Additionally, according to World Health Organization (WHO) guidelines, clinically eligible men who test positive for HIV should not be denied circumcision.9 During Kenya's first rapid results initiative for jumpstarting MC program in 2009, about 79% of the men who tested HIV-positive and knew their test results opted for circumcision.10

There is limited data on the effect of MC on plasma viral load or penile viral shedding, both of which may influence the transmissibility of the virus from HIV-infected men to their sex partners.11–14 In addition to breaching dermal integrity, MC causes inflammation, which can lead to increased penile viral shedding and increase the risk of HIV transmission.11,15–17 Wawer et al4 reported a significant increase in plasma viral load (+0.20 log10 copies/mL, P = 0.002) within 4 weeks postcircumcision among ART-naive men. It is possible that the postcircumcision increase in plasma viral load could lead to increased viral shedding and higher infectivity,13,18,19 but no study has reported the effect of circumcision on penile HIV viral shedding. This prospective cohort study was designed to assess changes in CD4+ T-cell counts, HIV viral load, and penile viral shedding after medical circumcision of ART-naive HIV-positive men in Kisumu, Kenya.

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This study was nested within a larger study that enrolled 215 HIV-negative and 108 HIV-positive men to assess wound healing and resumption of sex after MC of adult males by the forceps-guided method.20,21 HIV-positive participants were recruited among men seeking MC at the UNIM Research and Training Center of the Nyanza Reproductive Health Society and through referrals from local HIV testing centers and clinics that serve HIV-positive men. Plasma and penile lavage samples for viral load determination were collected from HIV-positive participants on the day of circumcision, at subsequent weekly follow-up for 7 weeks, and finally at week 12. Since plasma viral load did not change from baseline to week 6 postcircumcision in the first 19 men, additional assays were not run. Viral load assays in penile lavage were done for the same 19 men and, because of budgetary constraints, only for the next 10 enrolled ARV-naive men. These sample sizes can detect 0.48 log10 copies per milliliter change in plasma viral load and 0.38 log10 copies per milliliter change in penile viral shedding at any time point at alpha = 0.05 and power = 0.8. All participants were also screened for HSV-2 using Kalon HSV-2 IgG enzyme-linked immunosorbent assay (Kalon Biological Limited, Andershot, United Kingdom). Participants provided written informed consent for each study procedure. The study was approved by the Institutional Review Board of the University of Illinois at Chicago and the Kenyatta National Hospital Ethics and Research Committee.

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Postoperative wounds were assessed by a clinician at each follow-up and certified healed based on healthy scar formation with no scab or opening along the incision line and no suture tracks.20,21 At each follow-up, participants were asked by a study clinician in a face-to-face interview if they had engaged in sex since surgery. Men who answered yes were prompted to provide the date of first postsurgical sexual intercourse and to provide details regarding condom use, type of partner, and HIV-related risk behaviors. Counseling on behavioral risk reduction, including postcircumcision abstinence was reinforced at each follow-up.

CD4+ T-cell counts were performed on blood samples collected from 108 men just before circumcision and at 2 weeks postsurgery, using BD FACSCount (Dickinson and Company, Franklin Lakes, NJ). Venous blood and penile lavage samples for HIV-1 RNA assay were collected just before circumcision (baseline), and at weekly intervals through 6 weeks of follow-up or until the circumcision wound was fully healed. The blood samples were collected in EDTA bottles and centrifuged at 1200 rpm for 10 minutes. To collect penile lavage specimens, 5 mL of phosphate buffered saline (PBS; pH, 7.2) was measured into a 50-mL sterile cup and 2.5 mL drawn in a fine tipped transfer pipette and used to irrigate the penile coronal area. This irrigation was repeated 3 times and the wash fluid drained back into the same 50-mL cup each time.22–24 Plasma and penile lavage samples were aliquoted into 1-mL sterile cryotubes then stored at −80°C until assay. At assay, after thawing, samples were vortexed and 1 mL was ultra-centrifuged for 1 hour at 16,400 rpm at 4°C to pellet the virus. Viral pellets were re-suspended using 1100 μL of the 1× PBS and tested using Cobas Ampliprep/Cobas Taqman (CAP/CTM) version 2.0 with lower threshold for detection of 20 copies per milliliter. HIV-1 viral RNA was quantified using HIV-1 QS, which compensates for effects of inhibition and controls the preparation and amplification processes. Samples of <1000 mL were diluted 1 in 2 with 1× PBS and ultracentrifuged to pellet the virus. Results were multiplied by the dilution factor.

Viral load assays were done at Centers for Disease Control and Prevention HIV-Research laboratory in Kisumu that is ISO 15189 accredited and whose viral load platform is certified by the Virology Quality Assurance Program and College of American Pathologist.

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Statistical tests were done using STATA version 9.0 (StatCorp, College Station, TX; and SAS version 9.2 (SAS Institute, Cary, NC). Change in CD4+ T-cell count from baseline to 2 weeks postcircumcision was analyzed using mixed-effects regression to account for missing data. There being no missing values, multivariate analysis of variance was performed to assess change in HIV viral load in plasma and penile lavage after circumcision through 6 weeks of follow-up. A correlation analysis was done to explore the relationship between plasma HIV viral load and penile viral shedding. The χ2 test was used to assess the association between baseline CD4+ T-cell count (categorized as low or high using a cutoff of 350 cells/mm3) and ART and viral shedding, respectively.

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Baseline characteristics of the 108 study participants are summarized in Table 1. Median age was 28 (IQR: 25–32) years, 58.3% of the men were married, 56% of the men reported having 2 or more sex partners in the past 1 year and 31.5% of the men reported consistent alcohol intake at least once per week. Of the 46 (43%) men with CD4+ T-cell counts ≤350 cells per cubic millimeter at baseline, only 16 (34.8%) men were already on ART. Overall, 41 (38%) of 108 men were already on ART and 81 (75%) of 108 men tested positive for HSV-2.



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CD4 T-cell Count

CD4+ T-cell count results were available for 107 men at baseline and 103 men at week 2 postsurgery because of 1 invalid test result at baseline and 5 missing samples at week 2. For the 37 men already on ART, mean CD4+ T-cell count remained unchanged from baseline (393 cells/mm3) to 2 weeks postcircumcision (396 cells/mm3); P = 0.81. Among ART-naive men, CD4+ T-cell count increased from 417 cells per cubic millimeter at baseline to 456 cells per cubic millimeter at week 2 postsurgery (P = 0.04). There was no correlation between CD4+ T-cell count and plasma viral load either at baseline (r = 0.02; P = 0.93) or at 2 weeks (r = 0.049; P = 0.84) for the 19 men whose blood samples were tested for both CD4+ T cell and viral load.

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HIV Viral Load in Plasma

Figure 1 shows plasma viral load results for 19 ART-naive men before circumcision and at weekly intervals thereafter for 6 weeks. There was a small insignificant decrease in plasma viral load from baseline (4.86 log10 copies/mL) to week 4 postcircumcision (4.65 log10 copies/mL); P = 0.178, and multivariate analysis of variance showed no change in plasma viral load from baseline to 6 weeks after circumcision; P = 0.36 (Table 2). One man stood out as an outlier with a progressive decline in plasma viral load throughout the period of follow-up. His CD4+ T-cell count rose from 300 cells per cubic millimeter at baseline to 409 cells per cubic millimeter after 2 weeks.





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Penile HIV Viral Shedding

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).



Baseline CD4 cell count (<350 vs ≥350 cells/mm3) was not associated with penile viral shedding (none vs any) (Fisher exact, P = 0.33) nor was viral shedding associated with HSV-2 serostatus (χ2, P = 0.27). Plasma viral load and penile viral shedding were correlated at week 1 (r = 0.60; P= 0.007) and at week 2 (r = 0.58; P = 0.009) but not thereafter.

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.



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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.

Regarding penile viral shedding, 5 (17%) of 29 men had detectable HIV viral shedding at baseline. Viral shedding before circumcision could have been associated with scratches, abrasions, or micro lesions of the penile skin, which have been found to be frequent in this population, but these were not detected in this study.26,27

Despite detecting no change in plasma viral load after circumcision, we found that penile viral shedding increased dramatically to a peak of 2.41 log10 copies per milliliter 1 week after circumcision and then declined steadily such that only 1 of 29 men had any detectable penile shedding at week 6, and he had returned to undetectable levels by week 7. Although penile viral shedding was correlated with plasma viral load during weeks 1 and 2, the correlation did not persist thereafter, indicating that plasma viral load is unlikely to be a useful predictor of penile viral shedding during the crucial period when some men may resume sex with an unhealed wound. These findings are consistent with the many studies showing HIV-1 compartmentalization between blood and other tissues, and they demonstrate that assessment of penile viral shedding is crucial for determining the risk of HIV transmission during the postcircumcision period.28,29 Given that in 96.6% of the men, no viral shedding was detected after full wound healing, it is reasonable to conclude that the postcircumcision upsurge in viral shedding was primarily because of local breach in epithelial integrity. We found no difference in viral shedding between men who resumed sex early and those who did not, suggesting that sexual intercourse does not result in a breach in the functional integrity of a healed wound to cause an upsurge in viral shedding.

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

In conclusion, we observed that CD4+ T-cell counts and plasma viral loads of ART-naive HIV-positive men in Kisumu did not change after circumcision. There was, however, a surge in penile viral shedding within 1 week after surgery, but levels of viral shedding declined thereafter and became undetectable within 6 weeks. While our results indicate that the increased risk of HIV transmission by HIV-positive men because of surgical circumcision is small and transient during the 6-week postcircumcision window, WHO guidance for MC programs to emphasize postcircumcision sexual abstinence for 6 weeks and to promote consistent condom use should be reinforced.

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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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HIV viral shedding; plasma viral load; male circumcision; HIV-infected men; Kenya

© 2013 by Lippincott Williams & Wilkins