Delays in presenting for tuberculosis treatment associated with fear of ...

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African Journal of AIDS Research 2011, 10(1): 25–36 Printed in South Africa — All rights reserved

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ISSN 1608–5906 EISSN 1727–9445 doi: 10.2989/16085906.2011.575545

Delays in presenting for tuberculosis treatment associated with fear of learning one is HIV-positive Valerie Møller1*, Ida Erstad1, Jane M Cramm2, Anna P Nieboer2, Harry Finkenflügel3, Sarah Radloff4, Tinashe Ndoro5 and Stella A Kwizera6 Rhodes University, Institute of Social and Economic Research, PO Box 94, Grahamstown 6140, South Africa Erasmus University, Institute of Health Policy and Management, PO Box 1738, 3000 DR Rotterdam, The Netherlands 3 ’s Heeren Loo, PO Box 647, 3800 AP Amersfoort, The Netherlands 4Rhodes University, Department of Statistics, PO Box 94, Grahamstown 6140, South Africa 5Rhodes University, Department of Psychology, PO Box 94, Grahamstown 6140, South Africa 6Walter Sisulu University, Department of Sociology, Private Bag X1, Mthatha 5117, South Africa *Corresponding author, e-mail: [email protected] 1

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A cornerstone of tuberculosis (TB) control is early diagnosis and treatment. The first hurdle that prospective TB patients must overcome is to present at a public health clinic for treatment. The Global Plan to Stop TB addresses the new challenges of the intersecting epidemics of TB and HIV, and it aims to cut the transmission chain by achieving early and effective treatment of all people with TB infection. This goal may be more difficult to achieve in practice. Findings from a representative community survey conducted in an area of high HIV prevalence in the Eastern Cape Province of South Africa suggest that patients must conquer fear of knowing their HIV status in order to present for TB diagnosis and treatment. A total of 1 020 adults residing in a low-income suburb of Grahamstown, Makana Municipality, participated in a questionnaire survey that probed attitudes and opinions about TB and HIV/AIDS-related issues. The respondents were presented with eight factors previously cited in the literature as causing delays in presenting for TB treatment at a public health clinic. The single largest proportion of respondents attributed delay to a fear of discovering that one is HIV-positive. While the vast majority of the respondents agreed that knowing one’s HIV status is a civic responsibility (‘the right thing to do’), half indicated that the lack of privacy during voluntary counselling and testing for HIV at a public health clinic acts as a disincentive. The evidence suggests that a fear of knowing one’s HIV status is a deep-seated anxiety that is often not openly acknowledged, and that it is intertwined with the stigma related to the ‘new’ TB associated with HIV and AIDS. It is crucial to allay this deep-seated fear in the general public so that South Africa’s integrated HIV and TB services, designed to accelerate control of the twin epidemics, are successful. Keywords: case-finding, diagnosis and treatment, HIV-status anxiety, tuberculosis, South Africa, stigma

Introduction The ‘new’ tuberculosis (TB) linked to the HIV epidemic has proved difficult to bring under control in South Africa (Van Rensburg, Van Rensburg-Bonthuyzen, Heunis & Meulemans, 2005). Stigma-related reluctance to seek early treatment may be one of the multiple factors that undermine TB-control efforts; its importance is highlighted in the results of a survey inquiring into public opinion on the reasons for delay in presenting at a public health clinic for TB diagnosis and treatment. South Africa has the world’s worst HIV and TB epidemics in terms of numbers of people infected, and TB is the most common notified cause of natural deaths in South Africa (Karim, Churchyard, Karim & Lawn, 2009). The 2008 national estimate of HIV prevalence among South Africans of all age groups was 10.6%, with about 5.2 million being HIV-positive (Shisana, Rehle, Simbayi, Zuma, Jooste, Pillay-Van Wyck et al., 2009); 301 902 new cases of pulmonary TB were reported

in 2007, and about 73% of all TB cases involved co-infection with HIV (South African Institute of Race Relations, 2009; World Health Organization, 2010). The cornerstone of TB control remains the detection and cure of new, infectious cases of TB under the directly observed treatment short-course (DOTS) programme (Pronyk, Kahn & Tollman, 2007; Karim et al., 2009). Testing represents the first hurdle in bringing TB under control. Diagnostic delay leads to an increased period of infectiousness in the community and exacerbates the disease in affected individuals (Sagbakken, Frich & Gunnar, 2008). The Global Plan to Stop TB, launched in 2006, addresses the new challenges of the intersecting epidemics of TB and HIV. It aims to control TB mainly by cutting the transmission chain, which should be achieved by early and effective treatment of all infected people (Lönnroth, Jaramillo, Williams, Dye & Raviglione, 2009). The HIV pandemic has reversed the advances made in global TB control. The rapid progression of TB in

African Journal of AIDS Research is co-published by NISC (Pty) Ltd and Routledge, Taylor & Francis Group

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HIV-infected individuals highlights the need for much faster identification of the infection. The chances of recovering from TB are dependent on how sick the patient is when effective treatment starts (Wood, 2007). In South Africa, the results of a rural case-finding study suggest that a large proportion of deaths from TB might go undiagnosed (Pronyk et al., 2007). It is therefore vital that patients with TB present quickly to health services that offer treatment. This article begins with a review of the relevant literature and introduces the research question. The focus here is on the multiple barriers (including HIV-related ones) that reportedly cause people to delay in presentation for TB diagnosis and treatment in developing countries. Next, we describe the research design, the characteristics of the sample, and the key questions posed in the community survey. After that, we report the results and establish that the most important factor for delay was attributed to a fear of discovering one’s HIV status. We present the profile of respondents attributing delay to HIV-status anxiety in terms of their personal characteristics and attitudes to HIV and TB. Finally, we discuss the survey results from both a methodological and substantive perspective, and draw conclusions about their significance in relation to South Africa’s national strategic response to HIV and AIDS. Literature review Delays in presenting for TB diagnosis and treatment The literature cites multiple interlinked factors that delay people’s presentation for TB diagnosis and treatment in developing countries. The barriers tend to be contextspecific and vary according to the setting (Khan, Walley, Witter, Shah & Javeed, 2005; Dimitrova, Balabanova, Atun, Drobniewski, Levicheva & Coker, 2006). The focus of our study is on the barriers that delay people’s treatment beyond those factors related to structural poverty (see Farmer, 1997). The structural-poverty-related barriers found in our community study have been explored elsewhere (see Erstad, 2007). The next sections review select literature on people’s delay in accessing TB treatment owing to structural barriers, diagnostic problems and alternative treatment, and stigma-related factors. Structural barriers Most studies consider the importance of structural barriers that delay TB diagnosis, including lack of monetary resources or transportation and the distance to public health facilities (e.g. Khan et al., 2005; Zhang, Liu, Bromley & Tang, 2007). Long waits at public health clinics are further disincentives to seeking treatment (Edington, Sekatane & Goldstein, 2002). However, researchers on the topic of delay have acknowledged that socio-cultural factors may be equally important and should not be overlooked (Ngamvithayapong, Winkvist & Diwan, 2000; Edington et al., 2002). Since our survey was conducted in an urban area, the focus was not on the physical limits to accessing public health facilities, such as distance and transportation costs.

Møller, Erstad, Cramm, Nieboer, Finkenflügel, Radloff, Ndoro and Kwizera

Delays associated with diagnosis, self-treatment and traditional medicine A number of studies have documented the time delay between signs of symptoms of infection and a person’s presentation for TB treatment (e.g. Long, Johansson, Lönnroth, Eriksson, Winkvist & Diwan, 1999; Kanyerere & Aase, 2005; Cambanis, Ramsay, Yassin & Cuevas, 2007; Dodor, Neal & Kelly, 2008). Long delays may be due both to patients’ delay in seeking care and to healthcare providers’ delay in correctly diagnosing the TB infection (Long et al., 1999) and following up the patient. Khan et al. (2005) report that misdiagnosis by local doctors, both allopathic and traditional, led to considerable delays before patients in Pakistan were properly diagnosed. On the side of the patient, ‘illness representation’ (the incorrect interpretation of symptoms) may lead to a delay in seeking treatment (Woith & Larson, 2008). Self-treatment with ‘dubious’ (Rintiswati, Mahendradhata, Suharna, Purwanta, Varkevisser & Van der Werf, 2009) home remedies and over-the-counter drugs from pharmacies have been found to account for diagnostic delays (Matebesi, Meulemans & Timmerman, 2005; Sagbakken et al., 2008). Edington et al. (2002) found that traditional beliefs about the cultural causes of disease in a rural community in South Africa resulted in delays in presentation to a hospital or clinic. Competition between Western and traditional medicine may delay treatment-seeking, with patients seeking care from different sources, such as traditional healers and pharmacies (Eastwood & Hill, 2004; Rowe, Makhubele, Hargreaves, Porter, Hausler & Pronyk, 2005). Contrary to these reports from Africa, a study of TB patients in Peru found that self-treatment with over-the-counter and traditional medicines did not delay treatment-seeking (Oeser, Escombe, Gilman, Friedland, Evans & Moore, 2005). The consequences of delay A study in rural areas of Limpopo Province, South Africa (Barker, Millard, Malatsi, Mkoana, Ngoatwana, Agarawal & De Valliere, 2006), documented a strong relationship between treatment delay, consultation with traditional healers, and treatment outcomes. TB patients who had consulted a traditional healer took longer to access anti-TB chemotherapy (median 90 days) than those who had directly sought out government-provided health services. Those who visited a traditional healer before beginning chemotherapy had a worse performance status and were more likely to die because of their infection. Similarly, in the Free State Province, Matebesi & Booysen (2004) identified the long delay before diagnosis as a factor negatively affecting adherence to TB treatment. HIV-stigma-related factors Public attitudes and stigma are often cited as important deterrents for seeking timely care. The association of the ‘new’ TB with HIV and AIDS (Bond & Nyblade, 2006) has proved to be a main source of stigmatisation in South Africa (Matebesi & Booysen, 2004; Møller & Erstad, 2007) and this is commonly cited as a factor that delays people’s presentation for treatment in high HIV-prevalence

African Journal of AIDS Research 2011, 10(1): 25–36

areas (Matebesi & Booysen, 2004; Dimitrova et al., 2006; Sagbakken et al., 2008). However, the impact of stigma on delays is disputed by some scholars. For example, Reniers & Tesfai (2009) argue that because the contact rate with health-services providers is greatest for TB/ AIDS patients, it is unlikely that HIV/AIDS-related stigma is an impediment to seeking care. However, they do not exclude that stigma delays health-seeking behaviour. In contrast, a large focus-group study conducted in a high HIV-prevalence area of Thailand found that community members labelled most HIV-negative TB patients as AIDS cases (Ngamvithayapong et al., 2000). Reportedly, a fear of AIDS affected healthcare-seeking for other health problems: “Alarmingly, society’s heightened awareness of AIDS and inadequate knowledge of TB may cause delay in seeking TB care” (Ngamvithayapong et al., 2000, p. 1418). Similarly, a study of TB diagnostic delay in the Western Cape Province of South Africa found that Xhosa-speakers equated TB with HIV (Skordis-Worrall, Hanson & Mills, 2010). The ‘new’ TB associated with HIV and AIDS is more likely to be seen as punishment for the transgression of social codes of conduct. In Ethiopia, people’s perception that infringements of cultural or religious rules caused TB infections added to stigma and victim-blaming (Sagbakken et al., 2008), as drinking alcohol, smoking and drug use were known to weaken the immune system, which in turn made individuals more susceptible to infection. Sexual activity was believed to weaken psychological defences and TB patients’ will to avoid ‘temptations.’ In the South African study reported here, excessive drinking and smoking were perceived to be major TB-risk factors more than some other factors commonly associated with TB, such as crowded living conditions and poverty (Møller, Erstad & Zani, 2010). Stigma associated with using integrated TB and HIV services TB-treatment facilities are considered optimal venues for delivery of voluntary counselling and testing for HIV (VCT) services which are critical to effective HIV prevention (Daftary, Padayatchi & Padilla, 2007). South Africa’s National TB Control Programme routinely offers VCT to all TB patients (Department of Health, 2000). Gebrekristos, Lurie, Mthethwa & Karim (2009) found that participating in integrated TB and HIV treatment services at a TB clinic allowed patients to resist HIV stigma and negotiate the disclosure of their HIV status. From a patient’s perspective, ‘hiding behind TB’ was a major strategy for coping with their HIV status and for resisting HIV stigma. In contrast, Daftary et al. (2007, p. 574) reported that “experiences of stigma and discrimination were clearly barriers to VCT. Many patients were afraid, for instance, of being seen at HIV clinics. The expectation of stigma overrode the potential benefits of treatment.” Regular visits to primary healthcare facilities may act as markers of HIV infection or AIDS illness (Deacon, 2005; Skordis-Worrall et al., 2010) and thus reinforce stigmatisation (Matebesi & Booysen, 2004). To avoid the stigma associated with visiting public health facilities, some patients make use of private healthcare facilities

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(Sagbakken et al., 2008; Skordis-Worrall et al., 2010), causing further delay in diagnosing TB and accessing treatment for it. TB and HIV-testing anxiety Lastly, apart from disease stigma, anticipation of the TB test outcome may lead to delays in presentation for care. Rajeswari, Muniyandi, Balasubramanian & Narayanan (2005) note that patients react badly to disclosure of their TB diagnosis; their distress may become manifest as worry, depression, or suicidal thoughts. While patient-friendly healthcare facilities and patient confidentiality are considered essential for successful TB and HIV-testing services, arrogance on the part of healthcare workers, in particular towards less-educated and lower-income patients, are cited as disincentives for patients to present for healthcare (Ngamvithayapong et al., 2000; Zhang et al., 2007; SkordisWorrall et al., 2010). Research question The literature on reasons for delays in TB case-finding (as cited above) is largely based on qualitative and retrospective studies conducted among healthcare workers and patients. In contrast, this study reports on a general population survey conducted in an urban setting which explored the perceived role of stigma-related factors among other barriers that are thought to delay presentation for TB diagnosis and treatment. Methods Survey site The research was conducted in a low-income, residential area of Grahamstown (Makana Municipality) in the Eastern Cape Province of South Africa; this small university town and education centre has no industry and a high rate of unemployment. The township of Rhini (estimated population 100 000), formerly reserved for black residents during the apartheid era, was chosen because healthcare professionals expressed concern that many cases of TB in the area are detected late. The Eastern Cape (population 6 648 000) is regarded as a region with a high level of TB/ HIV co-infection: 63 533 cases of TB were reported in 2008 and an estimated 58.8% of TB cases involved co-infection with HIV (South African Institute of Race Relations, 2009). According to the Grahamstown TB Care Society, a monthly average of 498 TB patients were on the DOTS programme in the first half of 2010. Research design The research proceeded in two stages: a pilot study using focus-group methodology was conducted in early 2006 to inform the design of a larger sample survey fielded in late 2007. Pilot study The pilot study explored people’s understanding of TB as an illness and its possible association with HIV/AIDS and HIV stigma. The aim was to cover a wide range of viewpoints on the subject. A total of 59 participants (22 men and 37

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women), drawn from different neighbourhoods in Rhini, participated in focus group discussions. Discussants were selected purposefully to participate in group discussions for: 1) community health workers, 2) TB patients in hospital, 3) high school pupils, 4) out-of-school youth, 5) middleaged women, 6) middle-aged adults, 7) older men and women, and 8) traditional healers. The findings are reported elsewhere in full (i.e. Møller & Erstad, 2006 and 2007). The focus group discussions guided the researchers in compiling the inventory of questions and attitude statements used in the main study and on the appropriate phrasing of the items. Sample survey An area-stratified proportional-to-size sampling design was applied to select the survey respondents in Rhini. The township was first divided into 26 neighbourhoods. Within each neighbourhood, every 10th household was targeted using a random starting point. Within each targeted household, a Kish grid was used to select the interviewee, an adult over the age of 18 years who had lived in Rhini for at least six months during the previous year. In total, 1 020 respondents were included in the survey. The fieldwork was carried out in November 2007. Personal interviews were administered by trained fieldworkers in the respondent’s language of choice, using a questionnaire schedule containing mainly closed-ended items. Research instrument The questionnaire used in the sample survey reviewed viewpoints and issues that emerged as salient ones during the focus group discussions. Each set of response options to the closed-ended items included one or two options that could be construed as linked to anxieties or stigmatising beliefs. This approach intended to weigh the significance of stigma-related factors against other factors that play a role in the control of TB. The questionnaire was translated into the local language, Xhosa, and covered views on TB-risk factors, case-finding, adherence to treatment, financial and other types of assistance to TB patients and their families, and disclosure. Some 50 items explored the respondents’ attitudes and beliefs related to TB and HIV/AIDS. Because the research was exploratory, different formats were used to probe the topics under study, including Likert scales, multiple-response items, agreement or disagreement with statements, and the selection of the statement (in sets of two statements) that best approximated the respondent’s own viewpoint. The questionnaire also replicated the index of HIV/AIDS-related stigma developed for the South African context by Kalichman, Simbayi, Jooste, Toefy, Cain, Cherry & Kagee (2005). The eight-item scale covered multiple dimensions of blame, shame, pollution, divine punishment, and enacted stigma (such as avoidance, discrimination and restrictions on freedom). The researchers were aware that some questions and statements put to the respondents might sow doubt and prejudice and thereby inadvertently amplify stigma (see Somma, Thomas, Karim, Kemp, Arias, Auer et al., 2008). To counter this problem, the questions were prefaced with facts


on TB and the prejudicial-attitude items were introduced as hearsay. Key questions Three key questions were posed relating to delays in seeking a diagnosis and treatment for TB. We first inquired about access to public healthcare (‘Which clinic do you and members of this household usually visit when sick?’) to check whether distance factors represented a barrier to treatment. We then inquired into the respondents’ perceptions of factors that delayed presentation for TB treatment. The multiple-response question read: ‘Most people know about the symptoms of TB (such as persistent cough, night sweats, loss of appetite and weight loss), but not all people go to the clinic straight away to see if they need treatment. What are the most important reasons why some people delay going to the clinic?’ Eight response options were given. In order of presentation, the options cited possible factors related to inconvenience, loss of income, fear of gossip, difficulties producing a sputum specimen, anticipation of a difficult TB treatment regimen, treatment interfering with one’s social life, fear of being told one is HIV-positive, and the need to first consult a traditional healer. Delay factors tend to be context-specific (Khan et al., 2005; Dimitrova et al., 2006). The eight options provided were based on the delay factors identified by the pilot study (Møller & Erstad, 2006 and 2007). A multiple-response format was chosen to frame the question. The literature regularly cites multiple obstacles that delay early detection of TB rather than a single overarching factor (e.g. SkordisWorrall et al., 2010). Therefore, it seemed appropriate to ask the survey respondents to identify several obstacles to approximate the real-life situation. Furthermore, we reasoned that the respondents would feel more comfortable when allowed to select multiple causes rather than being forced to name only one. The same design was used as in other probes, namely to confront respondents with HIV- and stigma-related factors within a larger set of options. To date, research into TB diagnostic delay has concentrated on structural barriers. We chose a single option — that is, long waiting times at the health clinic — to represent structural barriers. Rhini is served by health clinics that are for the most part within walking-distance for clients. Throughout South Africa, TB treatment services are offered free of charge at the primary-care level in the public health sector (Matebesi & Booysen, 2004). Other factors mentioned in the literature on TB diagnostic delay were intentionally excluded. We also discounted the ‘illness representation’ factor (meaning the incorrect interpretation of symptoms) (see Woith & Larson, 2008) by specifying instances of known TB symptoms. Our study focused on people’s attitudes rather than their knowledge of TB. The pilot study (Møller & Erstad, 2007) indicated that acceptable ‘community knowledge’ (Zhang et al., 2007) of TB could be assumed. Also excluded from consideration were delays attributed to patients seeking to become chronically ill in order to qualify for a disability grant; hence, the ‘perverse incentive’ topic was covered in a separate module (Møller, 2010).


Results We report the characteristics of the sample followed by our findings about the perceived reasons for delay in presenting for TB diagnosis and treatment. A profile of the respondents who endorsed HIV-related anxiety as the single most important delay factor is compiled from the sample’s characteristics and attitudes to TB/HIV co-infection and stigmatisation. Characteristics of the sample The median age of the respondents was 38 years, and women represented a sizeable majority (see Table 1). The single largest group in the sample had completed some secondary education. Just under half (48%) came from households earning less than R1 000 (~US$150) per month and 70% came from households that received a non-contributory social grant, which was means-tested. The church is an important opinion leader in the study area. 1 The majority of the respondents were members of a Christian church: three-quarters (77%) of the respondents reported that they attended church regularly or occasionally, and about 44% identified themselves as born-again Christians. A high proportion of the respondents said they had personal experience of TB. Almost one-third reported that a case of TB had occurred in their household, and at least four in

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ten had acted as treatment supporters by assisting a TB patient to take their medicine regularly. A higher proportion of the respondents considered HIV infection rather than TB infection to be a personal risk in their lives. Delay in presentation at public health clinics The key questions about presentation at local health clinics in the case of TB symptoms were put to the respondents at the beginning of the interview. Access to healthcare The first item aimed to establish whether distance was a problem resulting in diagnostic delay. Almost all 1 020 respondent households reported use of public health services, predominantly the clinic located in their neighbourhood. Less than 2% indicated they visited a private doctor, and two respondents reported they had never been sick. Thus, it can be assumed that physical access to a local clinic was not a barrier in most cases. Furthermore, it can be assumed that most of the respondents were familiar with the services provided by their local health clinic. Reasons for delay The second survey item, which is the focus of this article, asked respondents why individuals who suspected they were infected with TB delayed presenting for testing.

Table 1: Characteristics of the study sample (n = 1 020 survey respondents) % Age (years) (median: age 38) 18–30 32.1 31–49 39 ≥50 28.9 Males 27.1 Females 72.9 Education level: No formal education to some primary school 35.3 Some secondary school 39.7 Completed high school 25 Self-rated health: Very good or good 59.5 Average 22 Poor or very poor 18.5 Born-again Christian 43.7 Knowledge and experience of tuberculosis (TB): Has been informed about TB and knows the symptoms 70 Thinks he/she does enough to avoid infection with TB 52.8 There has been a case of TB in the household 32.3 Has assisted a person with TB to take their treatment 44.9 If asked, would be willing to act as a DOTS volunteer to assist family, neighbours, or friends to take their TB treatment 63.4 Personal risk assessment:* HIV infection 54.7 TB infection 31.8 AIDS-related stigma scale** (set of eight stigmatising beliefs): Endorses no stigmatising belief 38.3 Endorses 1 or 2 stigmatising beliefs 55 Endorses 3 or more stigmatising beliefs 4.9 *The multiple-choice item read: ‘People are exposed to many dangers these days. What do you consider to be the two greatest dangers that could happen to you among the following: a serious road accident, an unwanted pregnancy, assault/rape, infected with TB, infected with HIV, a prison sentence.’ Each respondent was allowed two choices. **According to Kalichman et al. (2005). See text of the article for a general description.

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Eight reasons for delays in seeking TB treatment were provided; these covered: anticipated inconvenience (long queues; difficult testing process), the burden of treatment (unpleasant side effects), financial difficulty (loss of income), social factors (separation from family and friends), traditional health beliefs (need to first consult a traditional healer), fear of co-infection with HIV (being told one’s HIV status at the clinic), and stigma-related anxieties (e.g. exposure to gossip). The exact phrasing of the response options is given in Table 2. The response options were read out to the respondents. Their choice of four factors for delay was recorded in the order of their mention. The respondents were then asked to identify the single most important factor for possible delay from among the four options they selected. The first-mentioned responses received in the first round of ‘votes’ identified the long waiting time at a public health clinic as the greatest obstacle, endorsed by 71.2% of the respondents (see first column of figures, Table 2). This finding is unsurprising as concrete factors such as convenience or inconvenience tend to be obvious choices in attitude surveys. Moreover, the public health services in South Africa are known to be severely overloaded. The second round of cumulated responses covered a wider range of factors; beyond inconvenience, the most chosen response options involved people’s anxieties about stigmatising gossip (54.9%) and the spectre of losing one’s job or livelihood (40.1%) (see second column, Table 2). The third round of cumulated responses referred mainly to anxieties about disruptions to one’s social and family life (34.1%), anticipation of unpleasant testing procedures (i.e. ‘They don’t want to cough into the specimen bottle’: 41.7%), and a difficult TB-treatment regimen (33.1%) (see third column, Table 2). It was only in the fourth round of cumulated responses that a large proportion of the total sample indicated that people delay because they might be afraid they will learn


that they are infected with HIV as well as TB (84.3%) (see fourth column, Table 2). A minority of cumulative responses in the fourth round also attributed possible delay to people first consulting a traditional healer before visiting a clinic (10.3%). Most important barrier The third survey item sought to summarise the response pattern for the possible delay factors. When asked to identify the most important of the eight options, the majority named the fear of learning one is infected with HIV (62.7%), followed at a distance by the fear of gossip (12.2%). All other options were endorsed by about 6% or less (see far right column, Table 2). Survey summary To summarise, the survey found that the majority of respondents believed that fear of learning one is HIV-positive is the main barrier to early detection of TB. However, the fact that this attribution was initially suppressed is a very significant finding from both a substantive and a methodological perspective. First, allowing respondents the option of multiple choices prior to asking them to single out the most important option overall served to avoid some methodological problems commonly encountered in studies of perceptions. In surveys conducted in the past, we observed that factors that are described in concrete terms tend to be more obvious choices than are intangible factors that have to be circumscribed in more abstract terms. This was also the case in our study, where the respondents initially identified the long queues at clinics as the main obstacle to testing for TB. Second, if our research design had not made specific mention of an HIV/AIDS-related disincentive to present for TB testing, and had not allowed sufficient space for respondents to identify that factor as relevant, our study

Table 2: Perceived reasons for delays in tuberculosis (TB) case-finding (n = 1 020 survey respondents). The question read: ‘Most people know about the symptoms of TB (such as persistent cough, night sweats, loss of appetite and weight loss), but not all people go to a clinic straight away to see if they need treatment.’ The response options were read out in the order ‘a’ to ‘h’ and each respondent selected four Most important Important reasons* reason** Reasons for people’s delay Cumulative percentages over four rounds of responses % Response round: 1st 2nd 3rd 4th g) ‘They are afraid they will be told they are HIV-positive’ 0.1 0.1 6.8 84.3 62.7 c) ‘They are afraid that people will talk about their visit to the clinic’ 11.5 59.4 72.2 72.2 12.2 d) ‘They don’t want to cough into the specimen bottle’ 1.2 19.8 41.7 43.1 6.3 f) ‘They are afraid that TB treatment will interfere with their social life’ 0 1.6 34.1 42.4 6.3 a) ‘There are long queues at the clinics’ 71.2 71.2 71.2 71.2 3.9 b) ‘They are afraid they will lose their job/income’ 15.9 40.1 40.1 40.1 3.4 e) ‘They are afraid that TB treatment will be unpleasant and difficult’ 0 7.4 33.1 34.9 2.8 h) ‘They first wish to consult a traditional healer’ 0 0 0.1 10.3 2 Do not know any reason for people’s delay 0.2 0.2 0.2 0.2 0.2 No response 0 0.3 0.6 1.4 0.2 *Important reasons: i.e. ‘What are the most important reasons why some people delay going to the clinic?’ The cumulative percentages should be read across. For example, option ‘c’ attracted support from 11.5% of the total sample of 1 020 respondents in the first round of votes; additional votes from other respondents increased support for option ‘c’ in the second round to 59.4% of the total sample, and so forth, until cumulative support reached 72.2% by the final round. **Most important reason: i.e. ‘Which, in your opinion, is the most important reason?’ The percentages should be read down. The column percentages add up to 100% or nearest.


might never have uncovered the hidden anxieties that are an obstacle to successful TB control in an era of HIV. Attitudes to TB/HIV co-infection and stigmatisation The findings about delays attributed to HIV-related factors (i.e. response options ‘g’ and ‘c’ in Table 2) are embedded in a broader set of attitudes to TB/HIV co-infection and stigmatisation — made up of personal opinions as well as attitudes attributed to the community. The findings for this set of items are shown in Table 3. Seven in ten respondents in the total sample identified excessive drinking and smoking as a TB risk ahead of other well-known factors, such as crowded living conditions and poverty.2 The majority also believed that those infected with TB were susceptible to HIV infection. However, few believed that infection with TB was exclusive to people living with HIV or AIDS. Almost twice as many thought that TB in HIV-infected individuals was treatable rather than fatal. With few exceptions, the respondents agreed that one should know one’s HIV status. A large majority thought a confidential HIV test should be offered to all TB patients, as TB could be treated more effectively if one knew one’s HIV status. However, slightly more than half the sample regarded lack of privacy during VCT as a disincentive to HIV testing. About nine in ten thought AIDS could be regarded as a chronic disease since antiretroviral drugs (ARVs) enable individuals living with HIV to lead longer and healthier lives. Regarding stigma-related beliefs, half thought that TB-infected persons would be disrespected (Table 3).

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Twice as many thought churchgoers were supporters of TB patients rather than rumour-mongers (see Table 3). There was little evidence of stigmatising beliefs about people living with HIV, judging by the scores on the index of HIV/ AIDS-related stigma. Almost four in ten said they endorsed none of the stigmatising beliefs; less than 5% endorsed more than three of the items (Table 1). The majority endorsed only one or two beliefs, and these were related mainly to restrictions on freedom for people living with HIV, which might be construed as justified HIV-risk prevention. Correlates of HIV-status anxieties that delay presentation for TB treatment Taking into account the personal characteristics of the respondents (as listed in Table 1), and the set of attitudes to TB/HIV co-infection and stigmatisation given in Table 3, we compiled a profile of the respondents who considered HIV-status anxiety as the most important delay factor. This profile emerged for the survey category ‘They are afraid they will be told they are HIV-positive’ (which was cited as the most important delay factor). The attribution was strongly associated with an older age, poorer self-rated health, being a born-again Christian, regarding drinking and smoking as a TB-risk factor, and perceiving TB and/or HIV infection as a personal danger (see Table 4). The survey category was also related to less willingness to act as a TB-treatment supporter and the perception that TB patients are disrespected. The respondents in this survey category identified lack of privacy during VCT at public health clinics

Table 3: Assessment of the respondents’ attitudes to tuberculosis (TB) and HIV (n = 1 020 survey respondents) % 71.3 People who ‘drink and smoke a lot’ are at risk of TB infection1 People stay on TB treatment because they ‘don’t listen when people gossip about them’ 2 38.2 Agreement with the statement — ‘Only people who are HIV-positive get TB’ 11.4 ‘Almost all people with TB develop HIV/AIDS’ 60.3 ‘If you have TB, people do not respect you’ 51.3 ‘All TB patients should be offered a confidential test for HIV’ 88.9 ‘It is the right thing to do to know your HIV status’ 99.3 ‘AIDS is now like high blood pressure or diabetes because it can be treated like a chronic disease with antiretrovirals’ 89.5 ‘There is no cure for AIDS as yet but antiretrovirals help people to live longer and healthier lives’ 95.1 ‘If people knew their status, their TB could be treated more effectively’ 96.6 ‘People do not want to know their HIV status because there is no privacy during VCT at health clinics’ 56.7 Opinion that comes closest to one’s own — ‘Some people say: Fellow churchgoers encourage TB patients to stay on treatment’ 63.7 ‘Others say: Even church members gossip if a person has TB’ 36.3 ‘Some people say: HIV-positive people can be cured of TB like other people’ 64.7 ‘Others say: HIV-positive people who get infected with TB are likely to die’ 35.3 Recommendation on HIV disclosure3 — Disclose to community 29.3 Disclose to family members only 68.3 No disclosure 2.4 1In response to an item that asked the respondents to identify the persons ‘most likely to get TB’ according to a given list of 16 characteristics related to housing, socioeconomic status, poverty and unemployment, childhood immunisation, HIV status, lifestyle and virtue. Each respondent selected four characteristics. 2 In response to a multiple-choice question on factors conducive to adherence to TB treatment. Nine response options were supplied and each respondent could endorse up to four. 3 The item read: ‘What would you recommend to a person living with HIV but not showing any symptoms: to keep it secret, to tell only family members, or to share this information with the community?’

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Table 4: Correlates of tuberculosis (TB) diagnostic delay attributed to fear of being told one is HIV-positive, i.e. portion of the respondents choosing most important delay factor: ‘They are afraid they will be told they are HIV-positive’

Average for the total sample Age (years): 18–30 31–49 ≥50 Self-rated health: Very good or good Average Poor or very poor Born-again Christian Not a born-again Christian Identifies excessive drinking/smoking as a TB-risk factor: Yes No ‘People stay on treatment because they don’t listen to gossip’ Yes Other reason ‘Only people who are HIV-positive get TB’ Agree Disagree ‘Almost all people with TB develop HIV/AIDS’ Agree Disagree ‘If you have TB, people do not respect you’ Agree Disagree ‘HIV-positive people can be cured of TB like other people’ ‘HIV-positive people who get infected with TB are likely to die’ ‘People do not want to know their HIV status because there is no privacy during VCT at health clinics’ Agree Disagree HIV infection considered greatest danger in life: Yes Other choice TB infection considered greatest danger in life: Yes Other choice Willing to act as directly observed treatment short-course (DOTS) supporter: Yes No *p-value according to Kendall’s tau (see Tables 1 and 3 for a fuller description of the indicators)

as a deterrent to wanting to know one’s HIV status and they stressed the inevitability of co-infection. Majorities believed that almost all TB patients become HIV-infected (68.2%) and that only those with HIV get TB (81.9%). However, more encouragingly, 71.3% agreed that HIV-positive people can be cured of TB. Discussion Interpreting the survey results In our community survey exploring attitudes to TB, 89% of the respondents cited fear of being told one is HIV-positive at the public health clinic as an important factor for delayed TB-treatment-seeking. Some 63% named HIV-status anxiety as the most important delay factor. This finding is extraordinary for two reasons, substantive and methodological.

% 62.7 57.9 62.8 67.2 58.6 68.2 70.2 67.3 58.9

p-value*

0.016

0.001 0.008

67 52.2

0.0001

57.7 66.6

0.005

81.9 60.4

0.0001

68.2 54.5

0.0001

69.8 55.5 71.3 58.1

0.0001

68.8 54.8

0.0001

68.5 55.8

0.0001

67.9 60.3

0.018

59.6 68.7

0.0001

0.0001

This community survey explored what is often considered a taboo subject and made extensive use of multipleresponse items to factor in stigmatising beliefs in relation to TB treatment. Attitude surveys often make use of multipleresponse items. Such items usually allow for two response options, less often for three. Given the complexity of factors that are typically involved in health decisions and practices, we allowed for up to four responses. Based on longer-term experience with multiple-response items, the first-mentioned option attracting the largest number of ‘votes’ in the first round of responses typically attracts additional support in the following rounds — and thus emerges as the most significant one overall. The results of our survey did not fit this pattern. The response option relating to anxiety about HIV-positivity received only a single vote before the third round of questioning. However, exceptionally, by the fourth


and last round of responses, this response option had attracted the largest number of votes overall. Finally, the respondents identified the anxiety associated with knowing one’s HIV status as by far the single most important factor among the eight response options. How should we interpret such an unusual finding? The literature states that diseases that are fatal and sexually transmitted are more stigmatised than others (Deacon, 2005). Until recently, the South African government’s denial of the HIV epidemic (Chigwedere, Seage, Gruskin, Lee & Essex, 2008) and its refusal to roll out antiretroviral treatment (ART) may have added to the stigma associated with HIV infection. One interpretation is that the fear of HIV-positivity, which delays TB diagnosis, represents a deep-seated anxiety that is suppressed even when attributed to other people and therefore this response only surfaced in the last round. Another, related interpretation is that the respondents suppressed a response option denoting an attitude that is taboo and projects HIV stigma onto prospective TB patients. This reluctance to immediately pinpoint an HIV/AIDS-related barrier to TB diagnosis and treatment may be used to distance oneself from danger (see Deacon, 2005). Many of the survey respondents (54.7%: Table 1) regarded infection with HIV as a personal risk. The phrasing of the option endorsed by almost nine in ten respondents, ‘They are afraid they will be told they are HIV-positive’ when visiting the public health clinic, suggests multiple dimensions or layers of trauma. The first of these is the shock of receiving bad news about one’s health or else the confirmation of one’s fears; second is the situation and manner in which this news is communicated — likely in a public space by an overworked health worker who might not be sympathetic; third, there is anticipation of the burden of the disease; and finally the stigma associated with the illness. Learning that one has TB and must undergo a strict treatment regimen for at least six months will come as a shock. Learning at the same time that one must live with HIV infection for the rest of one’s life will be doubly distressing. The adjustment required to adapt to such a new life situation may be overwhelming. By way of illustration, other survey results suggest this is the case. In a section on quality-of-life assessment, the respondents were asked to describe in their own words the ‘best’ and ‘worst’ time in their life.3 A health problem defined the worst time of life for 9.6% of the respondents (or 98 of the total sample): six respondents cited TB as the health problem, and 17 indicated that discovering they were HIV-positive or knowing they had to live with HIV represented the worst time in their life. The worst time in life for one respondent was when ‘I found out I am HIV-positive and people were laughing and talking about me.’ Of significance for the discussion here is that, without exception, all 17 respondents whose worst time of life was defined by learning their HIV status also selected ‘fear of being told you are HIV-positive’ as an important factor delaying presentation for TB diagnosis or treatment, and 63% in the group identified this factor as the most important barrier. The proportion of votes coming from this particular group of individuals with personal experience of

33

living with HIV carries a greater weight than their absolute number. Many South Africans have never known their HIV status even if they have been tested. In a large nationally representative population-based survey, 50.8% of South Africans over age 15 years had ever had an HIV test in 2008 (Shisana et al., 2009), but only 27.6% had knowledge of their HIV status, and 7.8% of the total sample had taken an HIV test in the past 12 months and knew their test result (Peltzer, Matseke, Mzolo & Majaja, 2009). AIDS denialism on the part of the government in the past may have made South Africans more cautious about undergoing an HIV test and knowing their status. The finding from our study on barriers to health-seeking suggests that this reluctance to know one’s HIV status also impacts on the early detection of TB cases. Routine HIV testing at health clinics User-friendly entry points for TB diagnosis and treatment are considered essential to bringing TB under control (Dimitrova et al., 2006) and to turning around reluctance in the general public to take an HIV test (Karim et al., 2009). Similarly, VCT is cited as an important strategy for HIV prevention and access to treatment (Shisana et al., 2009). However, another viewpoint is that VCT presents a major barrier to HIV treatment, particularly in some rural Eastern Cape communities (Steinberg, 2008). The visit to a clinic that offers VCT and the duration of the counselling session serve as markers of HIV infection, which is associated with stigma. Findings from our community survey in Rhini suggest that public health clinics that offer routine HIV testing on presentation for TB treatment might deter rather than attract prospective TB patients. Lack of privacy is often cited as a disincentive to visit health clinics and to undergo testing for either TB or HIV. In our study, the respondents thought people should know their HIV status, but they also pointed out that there was no guarantee of privacy when undergoing an HIV test. When they endorsed TB patients’ right to an HIV test, they did so in a statement that specified that the test would be ‘confidential’ (see Table 3). Similarly, the study of TB diagnostic delay in Cape Town found that “TB implied HIV” among the Xhosa respondents (Skordis-Worrall et al., 2010, p. 176) who also cited fear of stigmatisation as a delay factor and voiced concerns about privacy during TB testing. A mathematical model demonstrates that universal voluntary HIV testing and immediate treatment with ART could greatly accelerate transition from the present endemic phase of HIV to the elimination phase (Granich, Gilks, Dye, De Cock & Williams, 2009). Important to the discussion here, it is further argued that universal voluntary testing and treatment could reduce HIV-associated stigma and could substantially reduce the incidence of HIV-related disease and deaths, including that from TB (Corbett, Marston, Churchyard & De Cock, 2006). The South African government has recently introduced a new era in HIV prevention and treatment: a shift from VCT to HIV counselling and testing (HCT) (South African National AIDS Council, 2010). The campaign launched in April 2010 offers HIV testing to all patients at entry points in all health institutions instead of waiting for people to voluntarily

34

present. All public health facilities, both fixed and mobile, are to be equipped to offer HIV testing and provide ARVs. The target of the new HCT programme is to test up to 15 million people (almost one-third of the population) by mid 2011. Although a surge in HIV-testing was observed in the first months of the campaign (Kahn, 2010), by November South Africa’s health minister conceded that the campaign was not meeting its target (Hartley, 2010). The new HCT campaign underway represents a breakthrough for South Africa — it ends the era of government AIDS denialism. For the first time in South Africa, public HIV testing has been led by the country’s political leaders, including the president. Given that testing served as a trigger for HIV stigma in the past, the normalisation of the testing and treatment process may reduce some of the deep-seated anxieties associated with learning one’s HIV status, as found in our study. However, if the current HCT campaign does not address public sensibilities, such as privacy (Bodibe, 2010), it may backfire if South Africans choose to delay seeking care for other health problems in order to avoid the routine HIV testing. This type of situation was observed in Thailand (Ngamvithayapong et al., 2000). Conclusions Testing is the first hurdle in achieving control of TB infections. The integration of HIV and TB services and rapid and appropriate management of drug-resistant TB are crucial components of TB control. Our study found that psychological factors may equal or surpass the often-cited structural factors that delay presentation for diagnosis and treatment of TB. Our method of inquiry has revealed what may be a very deep-seated anxiety associated with HIV testing. The majority of respondents in the community survey identified fear of learning that one is HIV-positive as the most important delay factor in early presentation for TB treatment. Just as the stigma associated with HIV and AIDS has spilled over onto TB in recent times, the denialism that has hampered the control of the HIV epidemic in South Africa may have negatively impacted on the early diagnosis and treatment of TB. It is possible that the government’s policy shift on HIV and AIDS since 2008 may have somewhat assuaged the type of anxieties evidenced in our community survey (conducted in late 2007). The new HIV-testing initiative launched in April 2010 may succeed in further diluting HIV/AIDS-related fears and stigma. Our study was limited to a single community survey in the Eastern Cape and reports attributions to factors that might lead to delays in TB diagnosis and treatment. The country’s new HCT campaign provides a unique opportunity to find out whether the concerns raised in this article are real or unfounded. Further research on actual health-seeking behaviour is needed to learn whether real progress has been made in providing the user-friendly entry points for TB diagnosis and treatment, in part by helping to dispel clients’ HIV/AIDS-related fears and stigma. Until such time as fears of a TB/HIV diagnosis are allayed, all efforts to control the twin epidemics may be futile.


Notes 1

2

3

While information on respondents’ education level is routinely collected in attitude surveys, the focus group discussions conducted for the pilot study suggested that religious values were also important in shaping views on TB and HIV/AIDS-related stigma. Therefore, background information was collected on religious affiliation and religiosity as well as education. Being a self-reported born-again Christian served as a proxy variable indicating religiosity in our study. Moral and biomedical understanding of TB risk are likely intertwined. A follow-up study (Møller et al., 2010) found that heavy drinking and smoking in shebeens (unlicensed township liquor outlets) was associated with a risky lifestyle that can spread both TB and HIV. The self-reported born-again Christians in the survey reported on here were more likely than others to cite drinking and smoking as a TB-risk factor. The respondents were defining the anchors of a scale to measure their subjective wellbeing using Anamnestic Comparative Self-Assessment (ACSA), which was applied for the first time in a South African survey. Previously the ACSA measure had been pilot-tested among Xhosa-speakers using a convenience sample (Møller, Theuns, Erstad & Bernheim, 2008).

Acknowledgements — The project titled ‘TB, stigma and quality of life in the Eastern Cape,’ on which this article is based, was supported by a grant from South Africa-Netherlands Research Programme on Alternatives in Development. The authors were members of the international research team. The fieldwork for the sample survey was commissioned to Development Research Africa Proprietary Ltd (South Africa). The useful comments of two anonymous reviewers are gratefully acknowledged. The views are those of the authors and should not be attributed to the sponsor or others.

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