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Changes in Male Circumcision Prevalence and Risk Compensation in the Kisumu, Kenya Population, 2008–2013

Westercamp, Matthew PhD; Jaoko, Walter MD; Mehta, Supriya PhD; Abuor, Pauline BA; Siambe, Perez BA; Bailey, Robert C. PhD

JAIDS Journal of Acquired Immune Deficiency Syndromes: February 1, 2017 - Volume 74 - Issue 2 - p e30–e37
doi: 10.1097/QAI.0000000000001180
Prevention Science
Free

Background: Three randomized controlled trials showed that voluntary medical male circumcision (VMMC) reduces the risk of female-to-male HIV transmission by approximately 60%. However, data from communities where VMMC programs have been implemented are needed to assess changes in circumcision prevalence and whether men and women compensate for perceived reductions in risk by increasing their HIV risk behaviors.

Methods: Scale-up of free VMMC began in Kisumu, Kenya in 2008. Between 2009 and 2013, a sequence of 3 unlinked cross-sectional surveys were conducted. All individuals 15–49 years of age residing in randomly selected households were interviewed and offered HIV testing. Male circumcision status was confirmed by examination. Design-adjusted bivariate comparisons and multivariable analyses were used for statistical inference.

Results: The prevalence of male circumcision increased from 32% (95% CI: 26% to 38%) in 2009 to 60% (95% CI: 56% to 63%) in 2013. The adjusted prevalence ratio of HIV and genital ulcer disease in circumcised compared with uncircumcised men was 0.48 (95% CI: 0.36 to 0.66) and 0.51 (95% CI: 0.37 to 0.69), respectively. There was no association between circumcision status and sexual behaviors, HIV knowledge, or indicators of risk perception.

Conclusions: The conditions necessary for the VMMC program to have a significant public health impact are present in Kisumu, Kenya. Between 2009 and 2013, circumcision prevalence increased from 30% to 60%; HIV prevalence in circumcised men was half that of uncircumcised men, and there was no or minimal sexual risk compensation.

*Division of Epidemiology and Biostatistics, School of Public Health, University of Illinois at Chicago, Chicago, IL;

Department of Medical Microbiology, University of Nairobi, Nairobi, Kenya; and

Nyanza Reproductive Health Society (NRHS), Kisumu, Kenya.

Correspondence to: Matthew Westercamp, PhD, Centers for Disease Control and Prevention (CDC), 1600 Clifton Road NE, Atlanta, GA 30329-4027 (e-mail: mwestercamp@cdc.gov).

Support for the Circumcision Impact Study is from a contract to the University of Illinois at Chicago from FHI360 and the Male Circumcision Consortium (MCC), a partnership between FHI360, EngenderHealth, and the University of Illinois at Chicago working closely with the Nyanza Reproductive Health Society. The MCC was supported by the Bill & Melinda Gates Foundation.

The authors have no funding or conflicts of interest to disclose.

The views expressed do not necessarily reflect those of the Bill & Melinda Gates Foundation or the MCC partners. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of this article.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial License 4.0 (CCBY-NC), where it is permissible to download, share, remix, transform, and buildup the work provided it is properly cited. The work cannot be used commercially without permission from the journal.

Received May 12, 2016

Accepted August 26, 2016

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INTRODUCTION

Three randomized controlled trials (RCTs) showed that voluntary medical male circumcision (VMMC) reduces the risk of female-to-male HIV transmission by approximately 60%.1–3 The results of these trials and of numerous observational studies provided the evidence for international normative agencies to endorse VMMC as an important component of a comprehensive program to reduce incidence of HIV in high prevalence regions where most infections are transmitted heterosexually.4 Since then, posttrial follow-up studies of participants in the Kenya and Uganda trials have demonstrated that the protective effect of VMMC is sustained and possibly strengthened during 5 years or more, and modeling of findings from Orange Farm, South Africa, indicate that, 3 years after scale-up of a VMMC program, HIV prevalence among men in the community would have been 19% higher had there been no VMMC program.5–7 Despite these findings, doubts remain whether implementation of a VMMC program will have a significant impact on the HIV epidemic outside a clinical trial setting. There is concern that risk compensation (also referred to as behavioral disinhibition) will occur at levels sufficient to mitigate the biological protection conferred by VMMC.8–10 This is despite no or minimal evidence of risk compensation occurring in participants of the 3 RCTs,1–3 in the posttrial follow-up studies,5–7 or in a longitudinal study designed specifically to compare sexual practices in circumcised and uncircumcised men in a programmatic setting.11

In addition to risk compensation, concerns about the possibility that large-scale VMMC programs will not successfully reduce HIV prevalence at a population level are based on demographic health survey data that show inconsistent associations between circumcision status and HIV prevalence in several countries.12,13 Such results may be explained by uncontrolled confounding, wide-scale misclassification of circumcision status, and the problem of temporality (ie, men getting circumcised after they are HIV infected).14,15 Therefore, quality monitoring and evaluation from communities where VMMC programs have been widely implemented are needed. Such an evaluation will also address question of whether sufficient numbers of men will accept a surgical procedure that may entail pain and time away from work, a 6 week period of sexual abstinence, and disruption of normal activities.16–18 Certainly, uptake of VMMC in some regions has lagged behind expectations, raising concern that the promise of VMMC as an effective HIV prevention program is limited.19

To evaluate whether a community-based scale-up of VMMC is to be successful, it will be necessary to demonstrate that at least 3 conditions prevail: that men and women do not increase their sexual risk behaviors from before the program is scaled-up to after it achieves a significant proportion of men being circumcised; that circumcision is acceptable and significant numbers of men get circumcised; and that circumcision reduces the odds of HIV acquisition in such a community setting. Between 2008 and 2013, we conducted 3 random household surveys to assess VMMC uptake, changes in sexual risk behaviors, and the association between VMMC and HIV infection in Kisumu, Kenya.

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METHODS

Study Setting and Design

Kenya's VMMC program began offering free medical circumcision services in November 2008 with a gradual scale-up through 2009 as government strategies evolved.20 Through 2013, the program had circumcised more than 730,000 men, most within Nyanza province, and had reached over 85% of the goal of reaching 94% circumcision coverage nationwide.19

The Circumcision Impact Study was designed as a sequence of unlinked cross-sectional surveys designed to describe middle- and low-income Kisumu residents throughout maturation of Kenya's VMMC program. Kisumu municipality, Kenya's third largest urban area and an administrative capital and economic hub of Nyanza province,21 includes the urban center of Kisumu city, several large densely populated periurban settlements, and surrounding rural environments. Kisumu served as the site for 1 of the 3 RCTs of VMMC for HIV prevention,2 and is a center for a large number of HIV research initiatives.

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Survey Methods and Eligibility

Our 2013 survey was carried out between January and July and used the same methodology as the 2008–2009 baseline and 2011 survey, described previously.22 Briefly, 40 study clusters were randomly selected within the low- to middle-income areas of Kisumu municipality from preestablished nonoverlapping areas comprising 50–150 households with selection probability proportional to the estimated underlying population as provided by the Kenya National Bureau of Statistics.23 All households present in a cluster were identified and a simple random sample of approximately 38 households per cluster was selected. All households were considered for selection. At least 3 visits were made if no one was at home but no replacements were selected for absences or refusals.

All men and women aged 15–49 years sleeping in the house the night before the first study visit were eligible. Those who were contacted and agreed to participate were interviewed in the home or other private location, and a certified counselor completed rapid HIV testing. Participants consented to each activity separately and interviewers were sex matched to the participant.

The survey sample size was calculated for 80% power to obtain estimates with an acceptable level of precision (4%–5% margin of error) with a confidence level of 95% and a response distribution of 50%. We assumed a design effect of 3.5, an average of 2 eligible residents per household, and a 70% participation rate.

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HIV Testing

The HIV testing algorithm used adhered to the serial testing algorithm guidance by the Kenya National AIDS and Sexually Transmitted Infection (STI) Control Program using test kits approved by the Kenya Ministry of Health.24 Whole-blood sample collected by finger prick was first tested using Determine (Abbott Laboratories, Chicago, IL) rapid testing kits. In 2011, samples testing positive were retested with Bioline third generation (Standard Diagnosis, Yongin, Republic of Korea, Korea). Negatives were considered negative for HIV infection. Concordant positive results were considered positive for HIV infection. Discordant results were tested using Unigold rapid test kit (Trinity Biotech Plc, Bray, Ireland) with results considered final. Because of a change in Kenya's HIV testing algorithm, the Bioline test kits were not used in 2013. Instead, positive rapid results were confirmed with the Unigold rapid test kit and any discordant results were resolved by enzyme-linked immunosorbent assay test performed at the local Kenya Medical Research Institute laboratory. All participants were provided with pretest and posttest counseling according to Kenya national guidelines, and all individuals tested received their results.

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Questionnaires

Study instruments were developed in English based on previous research addressing HIV knowledge, attitudes, and behaviors in the same general population2,25–28 and translated into the dominant local languages, Dholuo and Kiswahili. Data were collected on demographic, sexual, and other behavioral risk factors, and a basic sexual history including details on all spouses and up to 3 nonspousal partners within the last 12 months. All interviews and study activities were performed by specially trained research assistants with Kenya national HIV counseling and testing certification.24 Questionnaire data were either entered in the field using a handheld computer and a digital form29 or on paper. Data collected on paper were double entered into the database.

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Analytic Methods

Unless specified, all analyses incorporate sampling weights. Bivariate comparisons used design-adjusted statistical tests for categorical variables (ie, Rao-Scott chi-square30) with Wald-type 95% confidence intervals (CIs). Multivariable analyses used design-adjusted log-binomial regression techniques to provide adjusted prevalence ratio (aPR) estimates.31 Estimated population totals are based on sampling weights poststratified32 to age and gender population totals provided by the 2009 Kenya national census.21 All statistical analyses were carried out using the R statistical language and environment with the “survey package.”33,34

All information, including circumcision status, STI treatment history, and symptoms, was based on self-report. Circumcision status was also assessed by genital examination. Agreement between self-report and visual examination was high: 98% (342/350) in 2009, 99% (1135/1140) in 2011, and 98% (933/949) in 2013. “Sexually active” was defined as reporting any lifetime history of vaginal or anal sex. Marriage/spousal relationships were defined inclusively as legal, religious, cultural, or informal unions in which a man and a woman regard themselves as married. Nonmarital regular, casual, and transactional sexual partnerships were self-defined and categorized by the participant.

Ethical approval was obtained from the Kenyatta National Hospital Ethics and Research Committee and the Institutional Review Board of the University of Illinois at Chicago.

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RESULTS

For our 2009 baseline survey, we randomly selected 1120 households resulting in the identification of 1361 eligible women and 1210 eligible men with 1087 (80%) women and 675 (56%) men located and agreeing to participate. In 2011, 1633 households were selected resulting in the identification of 1671 eligible women and 1540 eligible men with 1540 (92%) women and 1372 (89%) men participating. Finally, in 2013, we selected 1513 households identifying 1598 eligible women and 1442 eligible men with 1524 (95%) women and 1309 (86%) men participating (Table 1).

TABLE 1

TABLE 1

Between 2009 and 2013, controlling for age, we observed no significant change in the HIV prevalence in male and female residents of Kisumu (Table 2). Over this period, however, the prevalence of several HIV risk factors did change. Educational attainment in female Kisumu residents in 2009 increased from 39% (95% CI: 33% to 44%) having secondary or higher education to 49% (95% CI: 45% to 54%) by 2013, a significant increase not seen among men. As the proportion of young women in school increased, age at marriage and age at sexual debut also increased. From 2009 to 2013, the proportion of women who had ever been married decreased significantly from 73% (95% CI: 68% to 77%) to 68% (95% CI: 64% to 72%), and the proportion of women reporting sexual debut at ≤15 years decreased by approximately 18% from 38% (95% CI: 34 to 43) to 31% (95% CI: 28% to 35%).

TABLE 2

TABLE 2

In men, there was a decrease in the proportion reporting 2 or more sex partners in the previous 12-months, from 23% (95% CI: 19% to 28%) in 2009 to 17% (95% CI: 14% to 19%) by 2013. No change was observed in women. Condom use at last sex with nonspousal partner increased significantly from 2009 to 2013 for both men and women, with women reporting a 59% (95% CI: 55% to 64%) increase and men a 50% (95% CI: 44% to 61%) increase (Table 2).

From 2009 to 2013, prevalence of male circumcision (MC) increased steadily from 32% (95% CI: 26% to 38%) in 2009 to 49% in 2011 to 60% (95% CI: 56% to 63%) by 2013. Applying weighted estimates (see Methods), this increase in MC prevalence represents 30,106 (95% CI: 27,353 to 32,859) circumcisions between 2009 and 2013. The proportion of women reporting circumcised partners also increased significantly from 45% (95% CI: 41% to 50%) in 2011 to 54% (95% CI: 50% to 58%) in 2013. Partner circumcision status was not assessed in the 2009 survey. MC prevalence increased across all age groups of men: 88% in men 15–19 years of age, 84% in 20–24 years, 82% in 25–29 years, and 61% in men 30–49 years of age (Table 3). As MC prevalence increased in the population, signs and symptoms of STI decreased. Compared with 2009 (23%; 95% CI: 20% to 27%), fewer sexually active men reported a history of STI treatment in both the 2011 and 2013 (20%; 95% CI: 17% to 22%) surveys. Additionally, fewer sexually active men reported genital ulcer disease (GUD) in the last 12 months (Table 2).

TABLE 3

TABLE 3

Table 4 shows changes between 2009 and 2013 in sexual behavior, HIV knowledge, and risk perception comparing circumcised and uncircumcised men. Between 2009 and 2013, adjusted for survey period and age, circumcised men were significantly less likely than uncircumcised men to be HIV positive (aPR = 0.48; 95% CI: 0.36 to 0.66). They were also less likely to report GUD in the last 12 months (aPR = 0.51; 95% CI: 0.37 to 0.69). Over this period, there were no differences observed between circumcised and uncircumcised men in sexual behaviors, including number of sexual partners, condom use, and history of nonulcerative STI, or in knowledge about HIV or indicators of HIV risk perception (Table 4).

TABLE 4

TABLE 4

To assess possible risk compensation in men who were circumcised under the VMMC program, we restricted the 2013 sample to all men who were ever sexually active and compared those who were uncircumcised with men who reported being circumcised in a clinical setting between 2007 and 2013. The men circumcised under the VMMC program were much younger than the uncircumcised men (median 22 years versus 29 years) and consequently less likely to be married (35% versus 65%), a difference that is not significant after adjusting for age (Table 5). The aPR comparing the HIV prevalence in men circumcised under VMMC with those remaining uncircumcised (aPR = 0.50; 95% CI: 0.24 to 1.05; Table 5) was similar to the aPR observed for all circumcised men (aPR = 0.48; 95% CI: 0.36 to 0.66; Table 5), although not statistically significant (P = 0.08) because of the smaller sample size. The protective effect of circumcision observed for GUD remained strong and significant in the 2013 subsample analysis (aPR = 0.30; 95% CI: 0.15 to 0.61). Unlike men circumcised outside the VMMC program (Table 4), men circumcised under VMMC were more likely to have 2 or more partners (aPR = 1.43; 95% CI: 1.00 to 2.02). Otherwise, there were no differences in sexual risk behaviors or beliefs about circumcision and HIV risk that would indicate risk compensation (Table 5).

TABLE 5

TABLE 5

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DISCUSSION

While 3 RCTs of medical MC have demonstrated the protective effect of MC against HIV incidence, little information is available from communities after VMMC program scale-up. We conducted 3 randomized household surveys in Kisumu, Kenya over 5 years to assess uptake of medical MC, whether circumcision is associated with reduced prevalence of HIV, and whether behavioral risk compensation has occurred after years of promotion and uptake of VMMC. Between 2009 and 2013, the prevalence of circumcision among men aged 15–49 years in Kisumu rose from 32% in 2009 to 60% in 2013. This represents approximately 30,000 additional men circumcised over this 4-year period, indicating that uptake of circumcision was substantial, and that Kisumu was well on its way to achieving the 80% target set for the region by the Kenya National AIDS and STI Control Program35 and by the World Health Organization and the Joint United Nations Programme on HIV/AIDS for high HIV prevalence regions of sub-Saharan Africa.36 Regarding the age distribution of circumcision, models indicate that circumcising men who have not started sexual activity leads to the greatest population-level benefit in the long term, whereas circumcising 20- to 34-year-olds has the biggest benefit over the following 10 years.37 The results of our surveys show that the Kisumu VMMC program is achieving a close to optimal age distribution of circumcisions with the greatest increases in prevalence among 15- to 19-year-olds (from 22% to 68%), 20- to 24-year-olds (35%–64%), and 25- to 30-year-olds (35%–63%), with lower MC prevalence among 30- to 49-year-olds (53% in 2013) (Table 3).

Concerns about the possibility that large-scale VMMC programs will not successfully reduce HIV prevalence at a population level are based on national cross-sectional demographic health survey data that show inconsistent associations between circumcision status and HIV prevalence in several countries,12,13 although not in Kenya.38 The results of our cross-sectional surveys in Kisumu found that the association of circumcision with lower HIV prevalence is intact and similar to the protective effect shown by the 3 RCTs. In the Kisumu population, the aPR of circumcision and HIV was 0.48 (95% CI: 0.36 to 0.66) with just 4% HIV prevalence in circumcised men compared with 12% in uncircumcised men in 2013. Restricting analyses to men circumcised only since the scale-up of VMMC, the HIV prevalence is just 3% compared with 12% in uncircumcised men (aPR = 0.50; 95% CI: 0.24 to 1.05). Similarly, prevalence of GUD is significantly less in the clinically circumcised versus uncircumcised men (aPR = 0.30; 95% CI: 0.15 to 0.61).

Risk compensation or sexual disinhibition after VMMC could mitigate or even negate the protective effect of VMMC in reducing HIV infection if men and women increase risk in response to perceiving themselves at less risk of infection due to increases in the proportion of men circumcised in the community.8 We found no evidence of risk compensation occurring among men and women in Kisumu during the 5 years of our surveys. To the contrary, we found that men and women reduced their sexual risk behaviors. The proportion of men having sex with 2 or more partners declined significantly as did the proportion reporting a history of STI treatment, and condom use with last nonspousal sex partner increased significantly among both men and women. The only indication of possible risk compensation was among men who had been circumcised in a clinic since VMMC scale-up: a greater proportion (17% versus 14%) reported 2 or more sex partners in the last year—a difference that is statistically significant, but unlikely to have a significant impact on the protective effect of circumcision against HIV infection as indicated by the aPR of HIV of 0.50 among these circumcised men.

Our results showing no or minimal risk compensation are consistent with previous findings. Large cohort studies using data from RCT participants in Kenya,39,40 data from initial VMMC program implementation in Kenya,11 and RCT follow-up data from Uganda6,41 suggest that risk compensation after VMMC is absent or negligible, and is not likely to undermine the impact of circumcision on HIV prevention. In the RCT conducted in Orange Farm, South Africa, there was a significant increase in the number of sexual contacts in the VMMC group,3 but the protective effect of VMMC was unchanged after adjusting for differences in sexual behavior. In Kenya, Agot et al, found no increases in risky sexual behavior in VMMC or control subjects at the end of a 1-year cohort study. A 1-year follow-up study of more than 1300 RCT participants in Kenya by Mattson et al, also found no evidence of risk compensation after VMMC. Risk behaviors decreased over time in both the circumcision and control groups, and no differences in the incidence of gonorrhea, chlamydia, or trichomoniasis were found between the 2 groups. The most comprehensive study of risk compensation in a nontrial, VMMC scale-up setting was conducted by Westercamp et al. Despite significant increases in sexual activity in the youngest age group and decreases in HIV risk perception in the circumcision group, no evidence was found for risk compensation after VMMC: all risk behaviors decreased over time in both groups. Notably, condom use increased significantly in both groups, with much larger increases in the VMMC group.11 Studies in Uganda by Kong et al and Gray et al in posttrial follow-up of participants in Rakai also found no evidence of risk compensation.6,41

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Limitations

We evaluated cross-sectional, representative population data sampled serially over time. This is not equivalent to longitudinal trajectories of individuals, but is appropriate for answering our broader question of how a population exposed to a VMMC program has changed over time. The possibility of reporting bias due to reliance on self-reported information was minimized through the use of questionnaires developed specifically for this population, extensive training of study staff, and visual confirmation of circumcision status. In 2009, our inability to locate selected individuals and overlap with other community HIV testing initiatives impacted participation. Poststratification weighting based on well-established population parameters was used to help adjust for suboptimal participation; however, selection bias may have been introduced if specific groups were systematically excluded. The use of cellular phones to contact participants and coordination with community HIV testing programs improved participation in subsequent rounds.

Mathematical modeling of other data by Nagelkerke et al42 suggests that our 5-year posttrial surveillance period is likely not sufficient to observe population-level reduction in HIV prevalence attributable to a VMMC program. Therefore, some proportion of the decreased HIV prevalence among circumcised men observed may be due to self-selection of HIV-negative or lower-risk men for the procedure. Additional study at further time points and the inclusion of HIV recent infection assays or refined mathematical modeling incorporating our findings would be helpful in directly attributing population changes in HIV incidence to VMMC initiatives.

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CONCLUSIONS

The conditions necessary for the VMMC program in Kisumu, Kenya, to have a significant public health impact over the next 10–20 years were present in 2013. Between 2009 and 2013, circumcision prevalence increased from 30% to 60%; the adjusted HIV prevalence in circumcised men was half that of uncircumcised men; and no sexual risk compensation was exhibited. Based on these results and considering that Kenya's successful VMMC program has been sustained,43 we should expect significant declines in HIV prevalence to be demonstrable in this population within the next few years.

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Keywords:

circumcision; male; HIV infections; Kenya; sexual behavior; health surveys; risk compensation

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