Abstract
The sexualization of the HIV epidemic in South Africa has been used as evidence that unsafe medical injections are of minimal importance to transmission in Africa, because the country was thought to be free of unsafe injection risks. More recent observation reveals routine failures in infection control in South African maternity and paediatric wards and in public dental clinics. In one province at least one medical injection in five is administered with a used needle or syringe. Over 25% of new HIV infections identified in South African adults using the BED IgG capture enzyme immunoassay in 2005 were in individuals reporting they had not been sexually active in the past 12 months. Immunization injections received at public health facilities are associated with HIV infections in children, many of whom may have passed HIV to their mothers during breastfeeding. South Africa is one of few countries in sub-Saharan Africa not using auto-disable (non-reusable) syringes for all immunizations. Using resource scarcity as justification for needle reuse is ethically indefensible, as injection safety is a readily achievable goal.
INTRODUCTION
Prevention of patient-to-patient HIV transmission is an ethical priority in health care everywhere in the developing world; yet, in the Republic of South Africa, these risks are known to exceed tolerable levels. In an influential review, the World Health Organization's Schmid et al. 1 recently argued that, ‘in the absence of unsafe injections’ the high HIV prevalence in South Africa excludes the possibility that unsafe medical injections are important to the pandemic. However, subsequent information from national surveys and the findings of an investigation into health-care safety in public health facilities together suggest that nosocomial risks are substantial, instead notwithstanding South Africa's excellent standard of blood supply safety.
The purpose of this review is to present and evaluate the evidence of the extent of probable nosocomial HIV transmission in South Africa. To understand the extent of these risks, the quality of our evidence on clinical practice and the quality of surveillance for unexplained HIV infections must be considered. We also question common scientific assumptions about survey data and injection risks, assumptions that partly explain the omission of injection risks from consensus HIV epidemiology in Africa.
The threat of extensive nosocomial HIV transmission has been demonstrated in major outbreaks in Russia, Romania, Libya and several other countries. 2–4 Health-care procedures including intramuscular injections and intravenous infusions were implicated in hundreds of infections in each of these outbreaks. Importantly, these outbreaks only became apparent upon investigation into one or several unexplained HIV infections. For this reason, instances of unexplained HIV transmission should not be presumed to represent isolated lapses in infection control. In South Africa 12 reported cases of HIV in children with HIV-negative mothers have been linked to intravenous injections or intravascular cannulation, at institutions that were not subsequently investigated to identify other cases. 5 The limited surveillance in place to identify such cases identifies about two each year. The costs of searching for more linked infections where clusters of cases have been identified in South Africa may seem to be prohibitive, as the number of potential index patients attending implicated clinics will be far greater than in countries with low HIV prevalence. This impediment must, however, be kept in perspective, considering how readily infection control problems can be redressed, in comparison with other HIV transmission risks.
The perception that unsafe medical injections are rare in South Africa rests on confidence in health worker training and supervision, and compliance with existing safety guidelines. Judging from unsafe clinical practice noted recently in most health districts in the Free State province, however, many health workers in South Africa may underestimate the survival of infective HIV in a needle or syringe. 6 Reuse of injection equipment probably carries an HIV transmission risk five to seven times greater than the minimal risk from a needlestick injury, considering the difference in inoculum volume between a superficial jab and an injection. 7–9 Working under rationing pressures and without an accurate estimate for the HIV transmission risk in an individual injection may predispose a large minority of health workers to view single-use protocols for injection safety as unacceptably wasteful. 10
The risk from an individual unsafe injection is unclear, as the minimum infective dose for HIV in blood exposures is not known, and is not uniform. However, rapidly progressing epidemics among injection drug users (IDUs) indicate that the risk from syringe or needle reuse is serious. 11 The biological plausibility of HIV transmission through medical injections is confirmed by the detection of amplifiable virus in needles and syringes collected after intravenous, intramuscular and even subcutaneous injections administered to HIV-positive patients. 12,13 The magnitude of an individual injection risk depends on the prevalence of HIV in that clinical setting (greatest when many patients have progressed to terminal illness), the volume of blood to which patients are exposed (greater in an injection than in a needlestick injury), the time elapsed between blood-to-blood contact (less than half of the viable virus is lost in the first two hours outside the body at 44ºC in wet conditions, as in a rinsing pan) and the viral load of the index patient (highest in primary infection or at progression to AIDS and terminal illness). 14,15 Many of these high-risk conditions describe the clinical setting in South Africa, suggesting that if unsafe medical injections are common in this country, extensive nosocomial transmission should be inferred.
UNEXPLAINED HIV TRANSMISSION IN SOUTH AFRICA
Non-vertical and non-sexual HIV transmission is evident from the 2005 national HIV prevalence and behaviour survey in South Africa, which tested almost 16,000 adults and children for recent HIV infections, using the BED IgG capture enzyme immunoassay (BED). 16 The results were adjusted for the known tendency of the BED assay to misclassify AIDS cases as recent HIV infections. Among children no longer breastfeeding (2–14 year olds), the estimated annual incidence of HIV was 0.5%. As most immunizations are given by age 18 months, the non-vertical HIV incidence in younger children may be greater.
One-third of the adults participating in the BED assay reported that they had not been sexually active over the past year, and 27% of recent infections were observed in this group. In the developed world, our understanding of HIV epidemiology would be seriously challenged if adults reporting no sexual activity contributed 27% of recent infections. The 4.3% HIV prevalence observed in self-reported virgins is 23% of the prevalence in sexually active adults in 2005 (ages 15–49). This is consistent with a similar national youth survey conducted in 2003, which found that the prevalence of HIV in young adults not yet sexually active was 3.9%. 17
Rehle et al. question the evidence for non-sexual HIV transmission in the BED survey, but their objections are not well supported. They note that 3.1% of women and 2.5% of men with a recent HIV infection who report not having sex in the past 12 months nevertheless report having another sexually transmitted infection (STI) in the past 12 months. This volunteered information is notably inconsistent with the belief that social desirability bias explains a respondent's claim to have been abstinent, if that individual has recently acquired HIV infection. Six of the most prevalent STIs in South Africa (syphilis, gonorrhoea, chlamydia, trichomoniasis, bacterial vaginosis and candida) are often asymptomatic for months, and thus may come to the patient's attention long after they were sexually transmitted. 18 For many of those reporting abstinence over the past year to volunteer information concerning an STI is notably inconsistent with the belief that social desirability bias explains a respondent's claim to have been abstinent, if that individual has recently acquired HIV infection.
To aver that unexplained HIV infections implicate both adolescents and adults with denial concerning epidemiologically implicit behaviour, without having attempted to trace any such infection through exposures at identifiable clinics, remains the norm in research but may not be sensible. The under-reporting of recent sexual activity (social desirability bias) has been well documented in comparable face-to-face interviews in rural Zimbabwe. 19 The likely presence of family members during the weekend household survey interviews in South Africa may have imposed greater peer pressure to under-report sexual activity. However, these interviews were conducted in privacy as far as possible. A very high rate of misreporting sexual behaviour would be required to characterize non-sexual HIV transmission to adults as unusual in South Africa.
ROUTINE LAPSES IN INFECTION CONTROL
Health-care HIV transmission seemed unlikely even in light of the national survey data, until 2008, when the report from an investigation in the Free State province quietly noted that, among children two to nine years old, receiving immunizations in public health facilities carried an odds ratio (OR) of 1.6 for HIV infection (relative risk 1.8). 6 The OR for children with HIV-negative mothers was 1.0 (no effect), reflecting the timing of probable nosocomial HIV transmission. Most South African children are still breastfeeding when they receive immunization injections, and child-to-mother HIV transmission has been shown to occur through breastfeeding. 20,21 South Africa is one of the few countries in this region not using auto-disable (non-reusable) syringes for all immunization injections.
The same investigation identified another seven HIV-positive children with HIV-negative mothers, and in Thabo Mofutsanyana health district 4.8% of HIV-positive children had HIV-negative mothers. No search was made for more cases, although 20% of 25 health worker interviewees in this health district reported reusing syringes, and two of three injections observed by investigators in this health district were performed with reused needles. In addition to injection risks, across all maternity and paediatric wards 23% of instruments coming into direct or indirect contact with patients were visibly contaminated with blood. Similar risks were encountered in public dental clinics, where practice was notably inconsistent with dental health workers' knowledge of the risk of transmitting blood-borne diseases. Needles were reused in 22% of injections in dental clinics, and only 60% of critical items were autoclaved.
Infection control lapses in public dental clinics and in milk banks implicated in several children's infections have been pursued following this investigation. The more prevalent HIV exposures in unsafe medical injections and unsafe deliveries have been minimized by comparison. Perhaps as a result of this selective attention, problems with injection safety are still perceived here and elsewhere in Africa as a peripheral issue and a distraction from core HIV prevention activities.
INJECTION DRUG USERS
The core public health message that HIV is transmissible both through sex and through needle reuse has not been taught consistently in Africa, because injecting drug use (IDU) is perceived as uncommon. This cannot be said of Cape Town, where the prevalence of injecting drug use is near 1%. 22 In drug transshipment countries, including South Africa, IDU prevalence has been increasing since the 1990s. Although most injection drug users (IDUs) in South Africa are white, the prevalence of injecting among black youth is rapidly increasing, and between 2002 and 2008 the national prevalence of IDU rose almost 10-fold, to an estimated 44,900 users. 23
The HIV epidemic among IDUs in South Africa has only recently outpaced the nationwide epidemic, with HIV prevalence in IDUs ranging up to 20% in 2005. 24 These rates can be expected to change rapidly, as over 80% of IDUs surveyed in Cape Town share needles frequently. 11 Harm reduction resources such as needle exchange programmes do not yet exist (through mid-2009).
The government's focus is on controlling the supply of drugs through criminalization, but demand reduction is also supported, targeting youth and at-risk women. 24 The average age at the onset of heroin use in South Africa is 20, and sex work is almost universal in female IDUs. Sex workers and youth are simultaneously at the epicentre of concentrated and heterosexual HIV epidemics, and the potential for explosive HIV transmission in these risk groups represents a public health threat affecting non-users as well.
IDUs who share needles are also at high risk of acquiring other blood-borne infections, particularly hepatitis C virus (HCV). In South Africa low HCV prevalence has been cited as evidence that HIV transmission is not resulting from unsafe health care. 25 HCV outbreaks are often associated with unsafe injections that could also transmit HIV, and this indication of patient-to-patient HIV transmission is not common in Eastern and Southern Africa. 26 However, the HCV prevalence in South African IDUs falls in the lowest 2.5% of HCV infection rates in the world, indicating that HCV infection is not a reliable risk marker for needle sharing in this setting. 27,28 The spontaneous elimination of HCV is strongly associated with chronic hepatitis B virus (HBV) carriage in dually infected individuals, and HBV is highly prevalent in southern Africa. 29 Viral inhibition at the population level could explain why in South Africa, where chronic HBV infection is highly prevalent, the HCV prevalence among IDUs is exceptionally low. This would also explain why South African patients receiving unsafe health care are not often infected with HCV.
ETHICAL PERSPECTIVES
The practise of unsafe injecting raises serious ethical concerns. The most serious of these is the exposure to risk of HIV infection of vulnerable patients such as children. Children are not able to either understand the risk that these practices hold for them or to take measures to avoid this risk. The Principles of Non-Maleficence (the moral duty to prevent harm) and Beneficence (the moral duty to act to the benefit of a patient) require that every possible measure be taken to protect vulnerable patients in this regard. 30
In the case of adults (including IDUs) it could be argued that patients ought to accept a measure of responsibility for their treatment by insisting on the use of sterilized skin piercing equipment. Without the knowledge of safe practices and adequate levels of confidence and self-maintenance vis-á-vis health-care personnel, however, such autonomy cannot be expected of patients or parents, particularly in rural populations. The realization of such a situation in health-care settings in the developing world is, at this stage, no more than a far-off ideal.
Health-care workers who perform invasive procedures unsafely can be expected to justify the practice as inevitable, given the crisis in resource limitations that health-care services are experiencing all over the developing world. Lack of knowledge may also, in certain cases, be a problem. Although this is not very likely with respect to the absolute risk of harming the patient, health workers may underestimate injection risks, if they are understood by analogy to needlestick accidents that only rarely transmit HIV. The impossibility of offering resource scarcity as justification for needle reuse must be stated. The management of HIV, so often hampered by factors that are difficult, if not impossible, to control, can in this instance be achieved through straightforward interventions ensuring efficacious infection control. 31
RECOMMENDATIONS
The history of the management of the HIV/AIDS pandemic in South Africa has been marred by denialism and negligence on the part of policy-makers. 32 It is first and foremost to be hoped that the problem raised in this article will not, again, be ignored. Safe health care is feasible and ought therefore not to be a significant factor in the spread of HIV, as patient-to-patient transmission is currently threatening to become;
One way of preventing nosocomial HIV transmission is the use of auto-disable syringes, i.e. syringes that cannot be used more than once and that automatically disable themselves after a single use. Even under conservative estimates of the risk of nosocomial HIV transmission, the auto-disable syringe has been found to be cost-saving in a 2006–2007 operational study in KwaZulu Natal. 33 Health services in South Africa should seriously consider using this technology;
An educational programme officiated in schools, the media and adult education programmes about the dangers of nosocomial HIV infections ought to be devised to reach patients and parents, going beyond the provision of posters in some clinical settings. Demand reduction programmes combating injection drug use may also serve as one important channel for educating the public about minor blood exposures that can transmit HIV;
The reuse of other contaminated equipment for invasive medical procedures should not be forgotten in the push to ensure injection safety.
