Tuberculosis patients' reasons for, and suggestions to address non-uptake of HIV testing: a cross-sectional study in the Free State Province, South Africa

Effective co-management of tuberculosis (TB) and human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/AIDS) necessitates that TB patients undergo HIV testing as early as possible after TB diagnosis [1–3]. In South Africa, provider-initiation of HIV testing for TB patients came into effect in 2007 with the adoption of the provider-initiated testing and counselling (PITC) strategy in the Tuberculosis Strategic Plan, 2007-2011 [4]. Findings of a study amongst providers in the Free State Province indicate that almost all nurses (according to their own reports) recommend HIV testing to TB patients, not only at inception of TB treatment (88%), but at every contact (61%) with the patient until acceptance of the test [5]. Despite such commendable efforts, reports indicate that less than half of the registered TB patients accepted HIV testing in 2007 (43.1%) and 2008 (45.9%) [6]. Indeed, at 39%, South Africa achieved a much lower HIV-testing rate amongst TB patients in 2007 than some other sub-Saharan African countries (e.g. Kenya - 79%) also heavily burdened with TB-HIV/AIDS [7].

In April 2010, following limited success of existing HIV-testing policies, the South African government initiated a mass HIV counselling and testing (HCT) campaign aimed at identifying and treating as many eligible persons as possible - TB patients included - before June 2011 [8]. This step confirmed the concerns of government and other interest groups that, despite ostensible implementation of routine/provider-initiated HIV testing, too many TB patients are currently not undergoing HIV testing [1, 9]. Research is thus needed to identify obstacles to uptake, and to find ways to improve the rate of HIV testing by TB patients in South Africa. The reported research provides insight from a patient perspective into why routine/provider-initiated HIV testing has been less successful than might have been expected in the case of TB patients. This study follows previous reports on predictors of uptake of HIV testing amongst the same patient population [10, 11].

It is important to establish patients' views so as to gain an understanding of non-utilisation of health services [12], which also includes the non-uptake of HIV testing. Evidence from studies conducted among TB populations elsewhere indicates that non-uptake of HIV testing may be attributed to: (1) patient-/individual-level factors, including fear of HIV-related stigma, negative experiences during prior HIV counselling, perceived lack of privacy at HIV-testing facilities, and prior HIV testing [13–15]; (2) relational factors, such as having to seek sexual partners' consent before undergoing HIV testing [14]; and (3) health systems factors, including lack of routine offering of HIV-testing services to TB patients, shortages of HIV testing kits, limited availability of HIV counsellors, poor inter-TB-HIV clinic referral systems, and inadequate counselling skills among providers [16].

However, no research has as yet been conducted to establish patients' reasons for non-uptake of HIV testing in the Free State. Despite a decrease from 32.9% in 2008 to 30.9% in 2009, the province has recorded high rates of HIV prevalence amongst antenatal women since 2007 (range: 30.1% to 32.9%) [17]. Moreover, at 818 cases per 100 000 population in 2007, the province had the fourth highest incidence of TB in the country [18], with six in every ten (60.3%) TB patients testing HIV-positive [6]. Our study sought to identify non-tested TB patients and to explore their reasons for not undergoing HIV testing. We also report both tested and non-tested patients' suggestions regarding what can be done to encourage a greater number of TB patients to undergo HIV testing. The survey formed part of a larger 'fact-finding' research project to inform the development of an intervention to improve uptake of HIV testing by TB patients in the Free State [9].

Almost one-third (32.5%) of TB patients participating in our study had, by their own report, not undergone HIV testing. These patients' reasons for non-uptake of HIV testing mostly amounted to patient-/individual-level factors. It had not been foreseen that many of the untested patients would be 'undecided' about undergoing HIV testing. However, drawing from previous findings amongst pregnant women in the USA [22] and a quantitative analysis related to the current TB patient population [10] on the significant association between definite HIV-related knowledge and uptake of HIV testing, a possible explanation for the patients' 'indecisiveness' could be that they were not adequately informed about the TB-HIV link. In line with research in Cambodia [23], most of the total group of tested and non-tested patients in our study suggested that intensifying dissemination of TB-HIV information by health care workers would facilitate their uptake of HIV testing.

Alternatively, given that testing for HIV positions people as being 'at risk' [24], it is possible that patients who were categorised as 'undecided' actually had no intention of undergoing HIV testing - perhaps for fear of being portrayed as 'promiscuous'. Again, the possibility exists that some of these patients might in fact actually already have undergone HIV testing but did not wish to reveal this, or indeed wished to keep their HIV status secret. Our findings showed a substantial proportion of the patient sample to be worried about either contracting or already having contracted and unknowingly been spreading HIV. This seemed to be a reasonable concern since more than half of all patients by their own report had not used condom protection during their most recent sexual encounter. Hence non-tested patients' supposed 'indecision' could have been a way to avoid further interrogation from the interviewers.

As with studies amongst TB populations elsewhere [13–15], some patients in our sample had not undergone HIV testing because of fear of HIV testing as such or because of the anticipated consequences of testing HIV-positive, such as being stigmatised. The reality of these patients' fear can be tied to diverse factors, including psychological issues [25], interpersonal relationships [14], and/or socio-structural factors [26]. Following research among TB suspects and patients in Kenya, it was envisaged that the implementation of PITC for TB patients in high HIV-prevalence settings would not only scale up HIV testing, but would also contribute to the mitigation of fears associated with uptake thereof [27]. Yet, as seen in our study, patients' fear of HIV testing persists. By implication, routine/PITC alone may be insufficient towards scaling up HIV testing amongst TB patients. As suggested by patients in our study, there is a need to implement a supplementary broader ethos of motivation and support.

Though research has indicated that TB patients are generally enthusiastic about collaborative TB and HIV activities [28], some patients in our study were nevertheless unwilling to undergo HIV testing, explaining that they still needed to deal with the burden of TB. These patients might have been concerned about the possibility of negative interactions between jointly administered TB and HIV drugs. Indeed, dual administration of TB and HIV treatment may present challenges such as overlapping and additive toxicities [29, 30]. However, such potential challenges should be outweighed by evidence demonstrating the feasibility, effectiveness and tolerability of dually-administered TB and HIV therapy [31, 32]. There thus seems to be a need to (better) inform patients regarding the advantages of simultaneous treatment for TB and HIV.

Similar to findings of a Cambodian study [33], more than half of non-tested patients in the present study reported that it had not been recommended to them that they undergo HIV testing. The lack of standardisation of clinical records meant that verification of such reports was not possible. However, to the extent that these patient reports are true, such a lack of provider-initiation of HIV testing could have adverse implications for meeting the target of 100% HIV testing by TB patients by 2011 [4]. At the same time, given that it is widely believed and proclaimed that HIV testing should be recommended to all TB patients in high HIV-prevalence settings [2, 3, 34], the non-practice of provider-initiation of HIV testing raises concerns about health workers' professional ethics and/or training, support and supervision in respect of PITC for TB patients. Our exploratory research suggests that it is imperative for TB control programmes to focus more attention on the implementation of the PITC policy directive.

As far as improving uptake of HIV testing is concerned, most patients asserted that it could be increased by motivation and support of TB patients by both health care workers and significant others in their communities. Also, providing (more) TB-HIV information to patients was perceived to be a salient role for health care providers. Our findings align with evidence from research in Kenya, which established that combined facility and community efforts are feasible and do indeed contribute to the scaling up of HIV testing [27].

Convenience sampling of patients limits the extent to which the findings may be generalised to populations of TB patients beyond the four sub-districts surveyed in the present study. However, as previously mentioned, comparison revealed that the patient sample did not differ significantly from the larger population of TB patients in respect of key biographical variables including sex and age.

Like all research based on self-reports, the current findings are subject to bias. The possibility of interviewer bias such as unintentional errors resulting from interviewers omitting questions or misunderstanding respondents is acknowledged. To reduce such bias we exercised in-field quality control including the immediate editing of questionnaires for completeness and accuracy. Where necessary, patients were traced to provide or clarify missing information. Our study does however offer insight into TB patients' perspectives regarding non-uptake of HIV testing in a specific context.

An important question left unanswered by the current research is that one of the reasons for non-uptake of HIV testing during a current episode of TB might be that patients had been tested for HIV at an earlier stage but due to fear of stigmatisation or other reasons, wished to conceal that and keep their HIV status secret. Our research also did not fully investigate the roles of gender and age. While it was observed that male and older TB patients were less likely to report having been tested for HIV, the reasons for such tendencies and how they can be addressed need to be understood in order to develop appropriate interventions for groups at high risk not to test for HIV.

Our study found patient-/individual-related factors or personal reasons to figure prominently in TB patients' explanations for non-uptake of HIV testing. This finding contributes to efforts to understand the limited success, to date, of routine/PITC implementation in South Africa. The only health system-related factor that featured - albeit much less prominently - in the patients' accounts of their non-uptake of HIV testing, was the reported non-offer of HIV testing at PHC facilities.

The study findings suggest that from the TB patients' perspective, initiatives to scale up HIV testing by TB patients in the Free State need to consider additional measures to augment routine/provider-initiation of HIV testing. The surveyed patients expressed a need for (more) motivation by and support from both health care workers and significant others, including family, friends and the community. Health care workers also need to (more) consistently and repeatedly inform and educate patients about the link between TB and HIV.