This is the largest study of HBV, HCV and HIV among key populations in South Africa to be published to date. The study confirms earlier research highlighting the high HIV burden among these populations [12]. Most importantly, it documents the alarmingly high seroprevalence of HCV infection among PWUD/ID (46%).
Demographics
This study follows South African census distinctions of race. These remain because education, socio-economic status and socio-cultural norms continue to map onto apartheid-era categories to some extent. In 2015, 81% of the population self-defined as Black, 9% as Coloured, 8% as White and 3% as Indian/Asian. The Western Cape has the highest proportion of people classified as coloured (50% of the population) [37], explaining the proportionally higher number of coloured people in Cape Town in each demographic category included in this study.
MSM were recruited from existing, specialised fixed site sexual health clinics. These served people from a wide range of socio-economic circumstances, reflected in the comparatively higher number of white MSM (up to 44% in Pretoria) included in the study and the lower rates (1 to 6%) of people who reported homelessness.
SWs were recruited through a combination of fixed sites and mobile services. Nationally, 5% of SWs are estimated to be male, a figure relatively stable across provinces [31] but this was not reflected in the study (<1% SWs male). Low numbers of SWs reporting homelessness may be because income generated from SW provides a means of paying for accommodation. Another explanation may be that current SW services are not reaching homeless SWs.
PWUD/ID were largely recruited at locations where mobile needle and syringe distribution and collection services where provided. The higher numbers of men who use drugs included in this study reflects programmatic data that indicates higher numbers of men (between 87% and 90%) to be using substance use services [38]. The low proportion of females who use drugs in this and other local studies [17,44] is likely also reflective of the gender distribution of PWUD/ID. Female-specific barriers to services—including a lack of tailored services and higher rates of stigma and discrimination experienced by women who use drugs [39]—likely also affected the number of female PWUD/ID in this study. The need for gender-appropriate and specific HIV and HCV services for women who use drugs is increasingly recognised locally [40], regionally [41] and globally [42].
HCV prevalence
The HCV findings are anticipated yet alarming. Unsurprisingly, PWUD/ID carried the highest burden with some marked variation across the country. The extremely high rates of HCV seroprevalence in this group in Pretoria (72%) is possibly due to the relatively longstanding nature of this injecting community. Viraemic rates at the upper limit (75–80%) of what would be anticipated may point towards repeated infections [40]. Equally, HCV seroprevalence in MSM, with high HIV-HCV co-infection prevalence, is expected given the risks of HCV infection among MSM, especially in HIV positive MSM and MSM with a history of injecting drug use [28].
The almost non-existent HCV seroprevalence among SW is supported by the low rate of injecting drug use and high condom use in this sample.
The circulating prevalence of HCV genotypes 1a and 3a is similar to other countries where HCV infection is networked and predominantly spread through the sharing of contaminated injecting equipment among PWID [43,44]. However, of note in South Africa, genotype 5a (a unique and prevalent genotype [45]) was not found and this suggests that 5a circulates in the general population and not in PWUD/ID or other KPs.
HIV
Lower levels of self-reported HIV status compared with measured prevalence (25% and 37% respectively) has been documented previously in South African KPs [46]. The fact that 25% of participants indicated that this was their first health-screening (including HIV testing) may indicate that a large number of people were genuinely unaware of their status due to fears of testing or competing priorities. This discrepancy may also relate to reporting bias and internalised stigma, fear of knowing one’s status, fears of acknowledging positive status while not on ART [47].
Overall reported use of ART, at 84%, was below the 90% target for people living with HIV, but higher than the national average of 57% [48], likely a consequence of the fact that participants were accessed through HIV service delivery platforms. The wide range across cities and populations (from 11% in PWUD/ID in Cape town to 96% MSM in Pretoria) also likely reflects which services are being primarily accessed at the included organisations by the target populations. The relatively lower levels of ART coverage reported among PWUD/ID (51%) further likely reflects the numerous barriers affecting ART uptake [16] in this population.
HBV
The overall HBsAg prevalence of 4% is similar to the general population [45, 9]. This may seem somewhat surprising given that we would expect these high risk groups to show a higher prevalence than that of the general population. The lower than expected HBV prevalence may also reflect the effects of the childhood immunization programme. WHO recommends universal access to HBV testing and the introduction of hepatitis B vaccination, including birth dose vaccination, for the elimination of HBV [50].
Blood borne virus co-infections
A global systematic review and meta-analysis of the prevalence and burden of HCV co-infection in people living with HIV reported a 6% coinfection prevalence in MSM and 82% in PWID compared to 2% within the general population [51]. In comparison, our findings indicate 3% HCV co-infection prevalence in MSM living with HIV and 65% in PWUD/ID living with HIV. A South African study among antenatal attendees living with HIV found HCV prevalence of 0.1% [52].
Overall 2% (75/3 439) were HIV-HBV co-infected with similar prevalence in all 3 KPs: 3%, 42/1 528 in SWs; 2%, 15/746 in MSM and 1.5%, 18/1 165 in PWID).
The overall prevalence of HCV-HBV co-infection was less than 1% (28/3 439). Only 10 participants (<1%) were HCV-HBV-HIV triple-infected, all of whom where PWUD/ID (4% of PWUD/ID living with HIV). The number of participants who were co-infected with HIV/HBV or HIV/HCV, or HCV-HBV-HIV triple-infected (<1%) is cause for concern given the extent to which co-infections can accelerate and amplify disease [5]. There is therefore the need for screening for co-infections in KPs especially HIV-infected PWUD/ID.
Risk practices
Substance use
Substance use varied across sites and populations, with alcohol being the most commonly reported substance. A range of illegal and unregulated substances were also reported, most notably heroin. Substance use treatment data [38] shows that the majority of heroin used in South Africa is smoked, usually in combination with cannabis and other agents. Heroin is also the most commonly injected drug among PWID [24]. Methamphetamine use is relatively more common in Cape Town than in the other cities, and injecting has been documented [24]. The HIV and viral hepatitis risks related to heroin are largely through injecting, with heroin dependant people injecting on average four times per day [24]. HIV and viral hepatitis risks relating to methamphetamine use are either indirect, through sexual risk as a result of increased sexual risk taking, or direct, through injecting [53]. In this study, a small proportion of MSM across the three cities reported injecting drug use. Injecting of heroin as well as methamphetamine, the latter in the context of substance use and sexual encounters (Chemsex) takes place among sub-groups of MSM, however little has been published around this practice in South Africa [54]. Chemsex among MSM can be associated with unprotected anal intercourse, and in some instances with multiple sex partners. This can be for long durations (up to days), and has been identified as a risk factor for HIV and viral hepatitis in other countries [55,56]. No SWs recruited reported injecting, however, networks of SWs who inject drugs have been reached through harm reduction and sex worker programmes operating in Johannesburg. Risks involved in substance use are exacerbated by criminalisation of drug use, limited access to harm reduction services, and discriminatory treatment within healthcare services [57].
Sexual practices
Sexual practices, unsurprisingly, differed considerably between KP sub-groups. SWs were more likely to report recent sexual activity, multiple partners, transactional sex and substance use at last sex as well as having the highest reported condom use, in general. Local research among females SWs in South Africa has identified high reported levels of condom use in major metropolitan areas (89% in Cape Town and 84% in Durban) [58].
SWs in this study were least likely to report lubricant use in relation to receptive anal sex. Little data exists on the use of lubricant during anal sex among SWs. Data from a three city bio-behavioural survey among female SWs in Cape Town, Johannesburg and Durban showed that only a quarter of female SWs were aware of lubricant, with low levels of reported use [58].
The greatest regional variation in sexual practices was also seen among SWs. Those in Mthatha region were more likely to engage in high-risk sex, with lower condom use and a much greater propensity to engage in sex in exchange for goods and commodities. In contrast, those living in KZN, reported much higher condom use and almost exclusively received money in exchange sex. This is likely reflective of the more rural geographic setting of Mthatha in comparison with the other more urban metropoles. There is however, little data on SW sexual practices outside of large metropolitan areas.
MSM were most likely to have engaged in receptive anal sex in the past week, had relatively low reported use of condoms but high lubricant use and comparatively moderate substance use at last sex. High-risk sexual practices, particularly low levels of condom use have been identified among MSM in South Africa. HIV prevention services for MSM have been operational in South Africa for almost a decade in the cities where MSM were recruited from, where condoms and lubricant are distributed [59]. Pre-exposure prophylaxis for MSM is available from the clinics where MSM were recruited, however, experience of PrEP was not assessed, which may have influenced condom use.
PWUD/ID were least likely to have engaged in sexual activity in the last month and reported relatively high condom use at last sex. Surprisingly, substance use at last sex was moderate and comparable to MSM, however, due to the frequency of substance use among PWUD/ID with a substance use disorder, under reporting may have taken place. While data on sexual practices among PWUD/ID in South Africa is limited, international research reflects that sexual practices are influenced by a range of factors, including relationship status [60] and mental health.
Limitations
This study drew on individuals from the included KPs already accessing available HIV prevention services. This opportunistic sampling limits extrapolation to other members of the included populations, who may have less access to health services, including harm reduction, or to other cities or regions in the country. Another important KP group that was not addressed by this study were prisoners where both HIV, HBV and HCV prevalence in other global settings is known to be higher than in the general population [57,61,62].
The use of English for the questionnaire in a context of multiple different first languages (including Afrikaans, Xhosa and Zulu), and potential ad hoc translating by researchers, may have undermined accuracy of answers in the questionnaire.
Long-standing relationships between participants and research implementation organisations is likely to have impacted on reporting accuracy. However, reporting bias may have resulted in under- or mis-reporting of measures assessing substance use and sexual activity. This may have been especially marked in relation to activities generally associated with the KP the participant was not identifying as (for example, SWs may have been less comfortable reporting substance use than people identifying as PWUD/ID). Self-protective behaviours encouraged by implementing organizations (such as the use of sterile injecting equipment among PWUD/ID or condoms across all KPs) may also have been over-reported, resulting in an under-representation of risk practices, and an over-representation of harm reduction practices. The questionnaire did not assess frequency of use of the various substances enquired about thus limiting the insights into substance use within these populations.