Some adjustment for confounders was reported for 15 studies. Most studies adjusted for age and one or more factors from the following: sociodemographic factors (marital status, area of residence, ethnic group), sexual behaviour (number of sexual partners in lifetime, last year or last 4 months, contact with sex workers), and factors associated with the risk of transmission (condom use, presence of ulcerative STD). Details are given in the footnote to Table 1. The study by Barongo et al.  was stratified by area of residence for the crude analysis, but residence was included as a confounder in the multivariate analysis, and hence the study contributed only once to the meta-analysis of adjusted effects. In addition, one study reported no significant association after adjustment for confounders but no details were given  and the study was not included in the adjusted meta-analysis.
All the 15 studies reporting an adjusted RR found a protective effect of circumcision on HIV risk (RRs ranging from 0.12 to 0.8), and in 10 studies the effect was statistically significant (Table 1;Fig. 1b). In general, the effect of adjustment was to strengthen the association between circumcision and a reduced risk of HIV, with the adjusted RR being smaller than or equal to the crude RR in 10 of the 14 studies that reported both measures. For two studies from Mwanza [21,22], the adjusted RR showed a decreased risk of HIV among circumcised men, although the crude RR had shown a non-significant increased risk of HIV associated with circumcision. The four studies in which the adjusted RR was closer to one than the crude RR were the studies from the Ivory Coast [32,36] and of STD clinic attenders in Nairobi [38,40]. In each of those studies, the difference between the crude and adjusted RR was small (Table 1).
The adjusted analysis showed a slightly stronger effect than the crude analysis (pooled adjusted RR = 0.42; CI 0.34–0.54;Table 2). For the 14 studies reporting both crude and adjusted RR, the crude RR was 0.54 (CI 0.39–0.74) and the adjusted RR was 0.45 (CI 0.34–0.58).
Analyses were then stratified by type of population. The crude analysis showed little evidence of an association between circumcision and HIV in population-based studies (crude RR = 0.93, CI 0.71–1.21). Of these 12 studies, six adjusted for confounders. The crude RR was reported in five of the six studies and was similar to that for all population-based studies (RR = 0.90, CI 0.59–1.36). The adjusted RR showed a significantly decreased risk of HIV among circumcised men (adjusted RR = 0.56, CI 0.44–0.70, based on six studies;Table 2, Fig. 2a). There was no significant heterogeneity between these studies (P = 0.21). When analyses were restricted to cross-sectional studies alone, results were very similar (crude RR = 0.91, CI 0.63–1.32; adjusted RR = 0.55, CI 0.42–0.72;Table 2).
Among the 12 studies of men at higher risk of HIV (STD clinic attenders, truck drivers, tuberculosis patients and hospital patients), the crude RR was 0.27 (CI 0.22–0.33). Seven of those studies included adjustment for confounders, which had little effect on the effect estimate (adjusted RR = 0.29, CI 0.20–0.41;Table 2, Fig. 2b). All adjusted RR were 0.5 or less, but there was significant between-study heterogeneity (P = 0.03). Results for cross-sectional studies alone were similar (crude RR = 0.24, CI 0.20–0.29; adjusted RR = 0.24, CI 0.18–0.31;P value for heterogeneity 0.49;Table 2).
There was wide variation in study size, with the largest study  consisting of 6821 men (25% of the total subjects included in the meta-analysis), whereas the second largest study consisted of 2603 men . To examine the influence of the largest study on the meta-analysis, we re-analysed the data excluding this study. The resulting RRs were similar (crude RR = 0.52, CI 0.40–0.68; adjusted RRs = 0.42, CI 0.32–0.55), indicating that the study did not influence the meta-analysis unduly.
Funnel graphs of the data are presented in Fig. 3a and Fig. 3b. There is no evidence to suggest that smaller studies (i.e. those with a larger standard error) were more likely to report a positive association, indicating no evidence of publication bias (Begg's rank correlation test:P = 0.56 for the crude analysis;P = 0.24 for the adjusted analysis).
The effect of using the OR instead of the risk ratio was assessed by re-analysing the cross-sectional studies using the risk ratio. For these 18 studies, the crude OR was 0.51 (CI 0.37–0.69) and the crude risk ratio was 0.59 (CI 0.47–0.73). In the high-risk studies, in which the prevalence of HIV was higher, the crude OR was 0.24 (CI 0.20–0.29), and the crude risk ratio was 0.37 (CI 0.33–0.41).
This systematic review and meta-analysis provide compelling evidence that male circumcision is associated with a reduced risk of HIV infection in sub-Saharan Africa. The strongest association is seen among men at high risk of HIV, but circumcised men in the general population are also at significantly reduced risk after adjusting for potential confounding factors. This supports results from the previous meta-analysis , which included 33 studies from around the world, and found an overall crude OR of 0.60 (CI 0.45–0.80), with a stronger effect in high-risk groups (crude OR = 0.33, CI 0.26–0.43) than in general population groups (crude OR = 1.04, CI 0.77–1.41). This was a re-analysis of previously collected data and had several major limitations (no systematic literature review, lack of adjustment for confounding factors, and lack of exploration of heterogeneity), which have been addressed in the present analysis.
Overall, there was significant heterogeneity between studies, indicating that the magnitude of the protective effect varies between populations. We would, however, expect any protective effect of circumcision to be heterogeneous across different populations because of differences in a number of factors, including variations in sexual exposure to HIV, timing of circumcision, but particularly differences in the prevalence of STD. There is evidence that male circumcision protects against some ulcerative STD (particularly chancroid and syphilis) , which in turn enhance HIV transmission, and this could explain the greater protection afforded by circumcision in populations in which genital ulcer disease (GUD) is more prevalent. Indeed, several studies adjusted specifically for previous or current GUD, and as GUD is likely to act on the causal pathway, the effect of circumcision on HIV may be stronger than that estimated by an adjusted RR.
When the analysis was stratified by the type of population, heterogeneity was reduced substantially and was not significant in the population-based studies. There was still significant heterogeneity among the seven high-risk populations, and the lack of reliable and consistent data from those studies on other potential effect modifiers (such as penile hygiene) prevented further exploration of this heterogeneity. However, the studies all found a strong protective effect (RRs from 0.12 to 0.50), and although this is a wide range, it suggests that a substantial protective effect was a consistent finding in all high-risk populations.
The main limitation of observational studies is that the effect of circumcision on HIV infection may be confounded by factors that are associated with HIV risk, and that may differ between circumcised and uncircumcised men. It is therefore important to note that adjustment for confounding strengthened the association in all the population-based studies, and generally made little difference in the high-risk studies. This is not surprising, because most studies that reported behavioural patterns [21,27,28,30,33,34,42,49] found that circumcised men tended to report higher risk behaviours than uncircumcised men in the same population. This would tend to result in higher HIV prevalence among circumcised men if there were no protective effect of circumcision. It remains a possibility, however, that there is residual confounding as a result of behavioural or biological factors that are unknown or poorly measured in some studies.
Religion and ethnicity are potentially important confounding factors in those observational studies, because they are likely to be associated with both circumcision and HIV risk. Three studies explored this by stratifying analyses by religion. Among Muslims in Kigali, Rwanda , circumcision was associated with a protective effect (crude RR = 0.18, CI 0.02–1.20). Little association was seen among Christians (crude RR = 0.79, CI 0.50–1.23), although this could be because, unlike Muslims, most Christians were circumcised post-puberty. A study in Rakai, Uganda , where 98.5% of Muslim men were circumcised, found that among non-Muslim men, those circumcised before the age of 12 years had a lower risk of HIV compared with uncircumcised men (crude RR = 0.62, CI 0.29–1.28). Furthermore, in Mwanza, Tanzania , the association between circumcision and HIV was similar when results were re-analysed excluding Muslims. Therefore the evidence suggests that circumcision has an effect on HIV infection independently of the confounding effect of religion.
It has been suggested that prepubertal circumcision (performed for religious or traditional reasons) is more likely to protect against STD and HIV, whereas postpubertal circumcision is likely to be performed as a consequence of infections, such as balanitis . Only two studies included in the meta-analysis asked about age at circumcision [22,28]. In Rakai , the strongest effect of circumcision on HIV risk was seen among those circumcised below 12 years (adjusted RR = 0.39, CI 0.29–0.53). There was also a significantly reduced risk of HIV associated with circumcision between 13 and 20 years (adjusted RR = 0.46, CI 0.28–0.77), and a non-significant effect above 20 years (adjusted RR = 0.78, CI 0.43–1.43). In contrast, among men in rural Mwanza , circumcision before 15 years was associated with an increased risk of HIV (adjusted RR = 1.50, CI 0.57–3.90), whereas circumcision at age 15 years or older was associated with a lower HIV risk (adjusted RR = 0.37, CI 0.18–0.74). The reasons for these discrepant findings are unclear, and further work on the effect of age at circumcision on HIV susceptibility is needed.
The observational studies included in this meta-analysis cannot definitively establish a causal role for circumcision in protecting against HIV infection. It is biologically plausible that the foreskin may enhance HIV transmission both directly and indirectly , although there is little direct evidence for this. Causality also implies that circumcision occurs before infection with HIV, and we cannot be certain of this with retrospective data, although the studies that reported age at circumcision [21,22,28,42] indicated that it usually occurs by 20 years, and hence is likely to precede HIV infection.
The present analysis was restricted to studies of HIV infection in men. Therefore we were able to assess only the effect of circumcision on male susceptibility, and not on male infectiousness. However, the advantages of this restriction are considerable. First, an effect of male circumcision on susceptibility is arguably more plausible on biological grounds than an effect on infectiousness. Second, only the circumcision status of the study subject is needed, and not the status of partners, thus reducing the potential misclassification of exposure. Third, a study on the effect of male circumcision on male–female transmission is complex, because a woman may have had more than one male sexual partner, with differing circumcision status. However, recent data from Rakai have shown that among discordant couples in which the male partner was HIV positive, there was a non-significant reduction in the transmission rate if the man was circumcised (rate ratio = 0.44, CI 0.15–1.32), and this reduction in risk was statistically significant among couples with male HIV viral loads of less than 50 000 copies per ml .
Circumcision was determined by self-report in 16 studies, and by clinical examination in eight studies. For four further studies [35–38] the method of ascertainment was not clear. Validity of self-reported circumcision was assessed among factory workers in Mwanza . Of the 111 men who had reported they were circumcised, only 69% were found to be so on examination. Among the 91 men who reported themselves as uncircumcised, 94% were found to be uncircumcised on examination. This suggests that self-reported circumcision may overestimate the proportion of men circumcised in this population, and suggests that genital examination should be carried out whenever possible in future studies. Assuming this misclassification is non-differential with respect to HIV status, the effect would be to underestimate the association between the lack of circumcision and HIV. All but one study performed HIV tests by one or two enzyme-linked immunosorbent assay (ELISA) tests, with confirmatory Western blot for discrepant or indeterminate ELISA results. The remaining study  performed only one ELISA with no confirmatory testing. Overall, therefore, there is likely to be little misclassification of HIV results.
Meta-analyses are vulnerable to bias, as a result of their failure to identify all eligible articles and also because research yielding statistically significant results is more likely to be submitted and published. Therefore, even if all published studies have been identified, these may be only a subset of the studies actually carried out. However, this seems unlikely to cause substantial bias in the present review because studies of risk factors for HIV almost always examined a range of behavioural and biological risk factors, and it is unlikely that the published studies were biased in terms of finding circumcision as a risk factor. However, it is possible that if no association with circumcision was found, this was sometimes not mentioned in the paper. The results of the funnel plot suggest that publication bias was not a problem in this meta-analysis, although the existence of such bias cannot be excluded. It was decided to exclude conference abstracts from the review because it is probable that these are more likely to report significant than non-significant findings, and therefore the inclusion of abstracts might increase bias.
The 28 studies reviewed were from just eight countries, including nine studies from Kenya (seven of these from Nairobi) and seven from Mwanza Region, Tanzania. As expected, there were few studies from West Africa, where circumcision in most areas is almost universal, although 39% of men in the study in Ziguinchor region, south-west Senegal were uncircumcised .
To our knowledge, two further studies on the effect of circumcision on HIV infection have been published since our literature review. A cohort study of trucking company employees in Kenya  found a very similar effect to our summary measure for high-risk populations (adjusted RR = 0.25, CI 0.1–0.5). A recently published study of HIV-discordant couples from Rakai, Uganda  found that the rate of female–male transmission was significantly higher among couples with uncircumcised male partners compared with couples with a circumcised male partner (rates of 16.7 per 100 person-years compared with 0 per 100 person-years;P < 0.001).
The data from observational studies provide compelling evidence of a substantial protective effect of male circumcision against HIV infection in sub-Saharan Africa, especially in populations at high risk of HIV/STD. The continuing rapid spread of HIV infection, especially in eastern and southern Africa, suggests that the potential public health benefit of introducing safe services for male circumcision on a wider scale should be explored. However, there are many concerns around such an introduction, including the possibility that men may increase their risky sexual behaviour if they think circumcision confers a high degree of protection, as well as the risk of bleeding or infection, cost, and issues of cultural identity. Studies are therefore needed to examine the acceptability, feasibility and safety of introducing male circumcision as an HIV/STD prevention strategy in high prevalence areas where men are not traditionally circumcised. Results from one such study among the Luo people in Nyanza Province, western Kenya, who are traditionally non-circumcising, showed that 60% of men would prefer to be circumcised, and 62% of women would prefer a circumcised partner . In areas where male circumcision is acceptable to the local community, randomized controlled trials of male circumcision performed by trained health workers as part of a package intervention incorporating safe sex education are needed. Such trials would overcome the inherent limitations of observational studies, and provide reliable empirical evidence on the overall impact of the introduction of male circumcision on HIV incidence.
The authors would like to thank UNAIDS for funding this study, Michel Caraël and Stephen Sharp for advice, and Simin Bahrainipur for administrative assistance.
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Keywords:© 2000 Lippincott Williams & Wilkins, Inc.
Heterosexual transmission; HIV-1 infection; male circumcision; meta-analysis; sub-Saharan Africa