Factors associated with linkage to HIV care and TB treatment at community-based HIV testing services in Cape Town, South Africa
Factors associated with linkage to HIV care and TB treatment at community-based HIV testing services in Cape Town, South Africa
Sue-Ann Meehan 0 1
Rosa Sloot 0 1
Heather R. Draper 0 1
Pren Naidoo 0 1
Ronelle Burger 1
Nulda Beyers 0 1
0 Desmond Tutu TB Centre, Department of Paediatrics and Child Health, Faculty of Medicine and Health Sciences, Stellenbosch University , Cape Town , South Africa , 2 Amsterdam Institute for Global Health and Development , Amsterdam , The Netherlands , 3 Department of Economics, Stellenbosch University , Cape Town , South Africa
1 Editor: Marcel Yotebieng, The Ohio State University , UNITED STATES
Data Availability Statement: The authors have
uploaded a minimal anonymized dataset necessary
to replicate the study findings to Figshare
(electronic data repository). The database can be
found at the following link, https://figshare.com/s/
b6b3e6ee56a1d40cfaec. They have included the
database and the data dictionary.
Funding: The community-based HIV testing
modalities (stand-alone centres and mobile
services) described in this study was supported by
the President's Emergency Plan for AIDS Relief
Diagnosing HIV and/or TB is not sufficient; linkage to care and treatment is conditional to
reduce the burden of disease. This study aimed to determine factors associated with linkage
to HIV care and TB treatment at community-based services in Cape Town, South Africa.
This retrospective cohort study utilized routinely collected data from clients who utilized
stand-alone (fixed site not attached to a health facility) and mobile HIV testing services in
eight communities in the City of Cape Town Metropolitan district, between January 2008
and June 2012. Clients were included in the analysis if they were 12 years and had a
known HIV status. Generalized estimating equations (GEE) logistic regression models were
used to assess the association between determinants (sex, age, HIV testing service and
coinfection status) and self-reported linkage to HIV care and/or TB treatment.
Linkage to HIV care was 3 738/5 929 (63.1%). Linkage to HIV care was associated with the
type of HIV testing service. Clients diagnosed with HIV at mobile services had a significantly
reduced odds of linking to HIV care (aOR 0.7 (CI 95%: 0.6±0.8), p<0.001. Linkage to TB
treatment was 210/275 (76.4%). Linkage to TB treatment was not associated with sex and
service type, but was associated with age. Clients in older age groups were less likely to link
to TB treatment compared to clients in the age group 12±24 years (all, p-value<0.05).
A large proportion of clients diagnosed with HIV at mobile services did not link to care.
Almost a quarter of clients diagnosed with TB did not link to treatment. Integrated
(PEPFAR) through the Centers for Disease Control
(CDC) under the terms of co-operative agreement
number U2GPS000739. The content of this
publication is solely the responsibility of the
authors and do not necessarily represent the
official views of PEPFAR or CDC. The funders had
no role in study design, data collection and
analysis, decision to publish, or preparation of the
Competing interests: I have read the journal's
policy and the authors of this manuscript have the
following competing interests: The last author was
the principal Investigator of the co-operative
agreement that supported the community-based
HIV testing modalities described in this study. The
first and fourth authors were involved in the
management of the community-based HIV testing
modalities described in this study. All data
collection and interpretation was done according to
good clinical practice. The other authors were not
involved with the community-based HIV testing
modalities in any way and declare that they have no
community-based HIV and TB testing services are efficient in diagnosing HIV and TB, but
strategies to improve linkage to care are required to control these epidemics.
Globally, the ª90-90-90º target has been adopted to end the Acquired Immune Deficiency
Syndrome (AIDS) epidemic [
]. South Africa has the largest burden of human immunodeficiency
virus (HIV) worldwide, with 7.1 million individuals living with HIV [
]. More than 50% of
new tuberculosis (TB) cases are among HIV-infected individuals [
] and TB remains the most
common cause of death among HIV-infected adults[
]. The World Health Organization
(WHO) emphasises the need to integrate tuberculosis (TB) screening practices into HIV
Testing Services (HTS) [
]. The South African Department of Health strongly advocates that HIV
services should be used as an entry point for TB screening [
] as South Africa strives toward
identifying 90% of individuals with HIV and TB and getting 90% of these individuals started
on treatment [
In South Africa, utilization of HTS occurs predominantly at public health facilities [
Although anyone can test for HIV on their own initiative, public health facilities primarily use
a provider-initiated testing strategy, whereby health providers are required to recommend
HIV testing to everyone attending health facilities, regardless of whether they have symptoms
]. This has been shown to be effective in increasing the number of people who test for
]. However, specific subgroups, such as males, are underrepresented in health
], hampering access to HIV services for these populations.
Community-based HTS provided on a mobile basis or at stand-alone centres provide a
different service offering from the existing public health facilities. Mobile services are provided
from a mobile van and `pop-up' tents, set up in public spaces. Stand-alone centres are fixed
premises, but not attached to a health facility. Both mobile and stand-alone centres only
provide HIV testing and related health services. Public health facilities offer a wider range of
health services from fixed sites. Mobile services reach different populations compared to
facility-based services; they are more likely to reach males [
], youth ( 25 years) [
] and older
individuals ( 31 years) [
]. Compared to mobile services, stand-alone services have a
higher proportion of individuals who test HIV positive [
Linkage to care for individuals diagnosed with HIV and/or TB is essential for individual
treatment initiation and for reaching the UNAIDS target. While an estimated 86% of
HIVinfected South Africans know their status, only 56% were on antiretroviral therapy (ART) in
]. For TB, an estimated 25% of smear-positive TB patients never start treatment [
These data emphasise the gap between diagnosis and linkage to care and treatment for both
HIV and TB.
Linkage to care is sub-optimal. Linkage to HIV care is estimated at 55% from facility-based
provider-initiated testing [
], at 60% from facility-based self-initiated testing [
53% from community-based mobile services [
]. No known published linkage to care data
exists at stand-alone services. While community-based services can diagnose HIV and TB
among individuals who typically do not access public health facilities [
], there exists limited
data around linkage to HIV care and TB treatment from integrated community-based HTS.
In addition, most studies have focused on factors associated with linkage to care at
nonintegrated services. This study is different because it specifically investigates factors associated
with linkage to care at community-based services that have integrated HIV and TB testing.
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Moreover, in contrast to previous studies, that focused on demographic factors, e [
clinical factors, [
]; psychosocial factors, [
]; and health service determinants
] of linkage to care, we investigate the association between service type
(mobile and stand-alone services) and linkage to care.
In addition, there is a paucity of data from operational settings and a gap exists for linkage
to care data from routinely offered community-based HTS where HIV testing and TB
screening services are integrated. To address this gap, this study aimed to quantify linkage to care for
HIV and TB and determine factors associated with linkage to HIV care and TB treatment at
community-based health services that deliver integrated HIV and TB services in Cape Town,
Design and setting
This retrospective cohort study used routinely collected data from clients that attended
community-based HTS (stand-alone and mobile) between January 2008 and June 2012 in the City
of Cape Town Metropolitan district of the Western Cape Province of South Africa. This
district houses 66% of the provincial population. Within this district, HIV prevalence is estimated
at 5.2% in the general population [
], and there exists extremely high rates of both
HIV-associated and non-HIV-associated TB [
]. Among individuals 15±44 years, HIV and TB are
among the leading causes of death [
]. More than 100 primary healthcare facilities offer HIV
and TB treatment in the district [
]. This study was conducted within eight communities in
this district, all of which are characterised by low socio-economic status [
] and high HIV
] and TB disease burden .
In each of these eight communities, community-based HTS integrating HIV and TB
screening, diagnosis and linkage to care was provided at one stand-alone and one mobile
service. Stand-alone services were located in shopping malls or residential areas and were fixed in
one location for the duration of the study, while mobile services were provided from tents and
a caravan (mobile van), strategically set up at various locations within the community, such as
transport hubs and along busy thoroughfares. The locations for mobile services were selected
on an ad hoc basis and changed regularly over the course of the study period. Anyone could
walk in without an appointment and request an HIV test at either of the stand-alone or mobile.
Both services were identically staffed by a professional nurse, who provided daily management
and clinical services together with an enrolled nurse (provides health care under the
supervision of the professional nurses) and three trained lay counsellors, who provided counseling
and HIV rapid testing.
All clients self-initiated HTS and underwent pre-test counselling; they were
symptomatically screened for TB and consent was taken for an HIV test. All clinical services provided at
the mobile and stand-alone were in accordance with Western Cape provincial guidelines. A
client was diagnosed HIV positive if both the screening and confirmatory rapid test results
were positive. If the rapid screening test was positive, but the rapid confirmatory test was
negative (discrepant result), blood was drawn and sent to the National Health Laboratory Service
(NHLS) for an enzyme-linked immunosorbent assay (ELISA). The HIV rapid test results were
provided during post-test counselling. A client with a discrepant result received the
appropriate counselling and was recalled when their ELISA result was available, approximately a week
later. Clients diagnosed with HIV were offered a referral letter for HIV care at a public health
facility of their choice.
A TB screening tool was used to screen all clients for TB symptoms (cough 2 weeks,
weight loss >1.5 kg, drenching night sweats, fever). Clients who reported one or more
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symptoms were regarded as presumptive TB cases and two sputum specimens taken at least
one hour apart, were sent to the NHLS for TB testing according to the national TB testing
algorithm at the time (smear microscopy for all presumptive TB cases and culture for previously
treated individuals and smear-negative HIV-infected individuals). A client was diagnosed with
TB if the microscopy and/or culture result was positive. All clients with TB were contacted by
telephone, recalled to the HIV testing service and provided with a referral letter to a public
health facility of their choice to initiate TB treatment.
A health care worker contacted all clients diagnosed with HIV and/or TB by phone, to
confirm whether they linked to care or not. Linkage to HIV care and / or TB treatment was
defined as self-reported attendance at a public health facility for HIV care / TB treatment
within 3 months after being diagnosed at a community-based HIV testing service. If a client
reported that they had visited a public health facility for HIV care and/or TB treatment, the
healthcare worker recorded that they had linked to care. If clients could not be contacted by
telephone, at least three more attempts were made at various times of the day over a 3-month
period. Clients that could not be contacted by phone by a health care worker, to confirm
whether they linked to care or not, were considered to not have linked to care.
Throughout the study period, all clients diagnosed with TB were eligible for TB treatment
, but not all clients were eligible for ART. At the beginning of the study period (January
2008) all HIV-positive individuals who had a CD4 count of 200 cells/mm3 were offered ART
at the public health facility . In 2010, the policy changed and ART was offered to
HIV-positive individuals with CD4 350 cells/mm3  and to all individuals co-infected with TB,
irrespective of CD4 count . The study ended prior to the current guidelines (in which all HIV
positive individuals are offered ART regardless CD4 count) .
The study included data from clients who utilized the stand-alone or mobile services between
January 2008 and June 2012. At both services, healthcare workers routinely captured data of
each client on paper record forms; including demographic and clinical variables and linkage to
care. Each client record had a unique barcode for study purposes. Client records were kept at
the HIV testing service for three months before being transported to a central data office. A
Microsoft ACCESS 2013 database was specifically designed for this study. Two independent
data clerks entered data into two separate datasets, after scanning the client's unique barcode
into the dataset. After comparing the two datasets, a third data clerk validated any differences
after referring to the source data (paper forms). This resulted in a final anonymized dataset,
with no individual identifiers. All clients 12 years, who had an HIV test done and a
documented HIV test result, were included in the analysis.
This study had two primary outcomes of interest: 1) linkage to HIV care among clients
diagnosed with HIV at HTS; 2) linkage to TB treatment among clients diagnosed with TB at HTS.
Determinants (sex, age, HIV testing service and co-infection status) were identified using
logistic regression. Generalised estimating equations (GEE) were incorporated to control for
correlated data (two HTS services were located within the same community).All variables were
included in the multivariate analysis, irrespective of their association with the outcome in
univariate analysis. The level of significance in all analyses was p<0.05. Analyses was completed
in Stata (StataCorp. 2015. Stata Statistical Software: Release 14. College Station, Texas, USA:
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The Health Research Ethics Committee of Stellenbosch University (N08/10/307) approved the
study, which was conducted according to the guiding principles within the Declaration of
Helsinki. All clients who underwent an HIV rapid test provided written consent on their client
record form. No incentives were provided.
Linkage to HIV care
Overall 79 545 clients, with a known HIV test result were included in the study, of which 39
142 were males. The median age of all clients was 29 years (IQR 22±41).
Of the 79 545 clients who had a known HIV test result, 5 929 (7.5%) were diagnosed with HIV
(1 870 at stand-alone and 4 059 at mobile). Of these 3 738 (63.1%) were linked to HIV care (1
311 at stand-alone and 2 427 at mobile). See Fig 1. Among males, 1 388/2 159 (64.3%) linked
to HIV care. The median age of clients linked to HIV care was 30 years (IQR: 25±37). Among
clients co-infected with TB, 59/86 (68.6% linked to HIV care. At the stand-alone service,
linkage to HIV care was significantly higher as compared to linkage to HIV care at the mobile
service (70.1% vs 59.8%, p<0.001) (Table 1).
Compared to clients diagnosed with HIV at stand-alone services, clients diagnosed with
HIV at mobile services had a significantly reduced odds of linking to HIV care (aOR 0.7 (CI
95%: 0.6±0.8), p<0.001 (Table 2). Linkage to HIV care was not associated with sex, age or TB
co-infection. Multivariable analysis in S1 Table shows that linkage to HIV care at both the
stand-alone and mobile modalities were not associated with sex, age or TB co-infection.
Linkage to TB treatment
Of the 79 545 clients with known HIV status, 50 were excluded from the analysis as no TB
symptom screening was done. Of the 79 495 clients screened for TB, 5 079 (6.4%) were
presumptive TB cases, of which 4 341 (85.5%) were tested for TB. Of those tested, 275 (6.33%)
were diagnosed with TB (155 at stand-alone and 120 at mobile). The majority (76.4%) linked
to TB treatment (121 at stand-alone and 89 at mobile). See Fig 2.
Among males, 121/165 (73.3%) initiated TB treatment. Clients who initiated TB treatment
were younger (median age 29 years, IQR: 25±41) compared to those who did not initiate TB
treatment (median age 36 years, 95% CI: 27±45) (p 0.007). Among clients co-infected with
HIV, linkage to TB treatment was higher as compared to linkage among those without
coinfection (84.9% vs 72.5%, p = 0.025). See Table 1.
Table 2 shows that linkage to TB treatment was associated with age. Clients in the age
groups 25±34 (p = 0.046), 35±44 (p = 0.007) and 45 years (p = 0.019) were less likely to link
to TB treatment compared to clients in the age group 12±24 years. Linkage to TB treatment
was not associated with sex, HIV testing service or HIV co-infection. At the stand-alone,
linkage to TB treatment was not associated with sex, age or HIV co-infection. At mobile, clients in
the age groups 25±34, 35±44 and 45 years were less likely to commence TB treatment
compared to clients in the age group 12±24 years (all, p-value<0.02). See S1 Table.
This study quantified linkage to HIV care and TB treatment and determined factors associated
with HIV care and TB treatment at an integrated community-based HTS, offering HIV testing
and TB screening and testing from stand-alone and mobile services. Linkage to HIV care was
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Fig 1. Linkage to HIV care for clients with known HIV status at community-based HIV testing services in the City
of Cape Town Metropolitan district, Western Cape, South Africa.
63.1% and was associated with service type (at the stand-alone service, linkage to HIV care was
significantly higher as compared to linkage to HIV care at the mobile service). Of those
diagnosed with TB, 76.4% linked to TB treatment, which was associated with age (clients who
initiated TB treatment were younger compared to those who did not initiate TB treatment).
Linkage to HIV care in this study is higher than what has been reported from mobile
services in other Cape Town studies (51%-53%) [
]. Studies use different definitions of
linkage to care, making comparison difficult.
Our study found that the type of HIV testing service (mobile or stand-alone) was associated
with linkage to HIV care. This differs from a study in Swaziland, that found that the type of
HIV testing service (home-based compared to mobile) was not associated with linkage to HIV
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PLOS ONE | https://doi.org/10.1371/journal.pone.0195208
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Fig 2. Linkage to TB treatment for clients with known HIV status at integrated community-based HIV testing
services in the City of Cape Town Metropolitan district, Western Cape, South Africa.
]. In our study, mobile services diagnosed and linked more clients to HIV care than
the stand-alone service (2 427 clients at mobile and 1 311 clients at stand-alone were linked to
care), indicating the important role that mobile HTS play in diagnosing and linking large
numbers of individuals with HIV. However, clients diagnosed with HIV at mobile services
were significantly less likely to link to care (59.8%) as compared to those diagnosed at
standalone services (70.1%). This finding emphasises the need for improved linkage to HIV care
interventions and suggests that efforts to improve linkage to care from mobile could have a
significant impact on increasing linkage to care overall. Interventions that provide client support
after diagnosis, including additional counselling and accompanying the client to the health
facility may improve linkage to HIV care. Future operational research studies should compare
different interventions at mobile services to determine more efficient linkage to care.
Awareness of symptoms of disease has been associated with voluntary uptake of counselling
and testing [
]. Awareness of disease may also play a role in linkage to care. Clients who
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accessed a stand-alone service for an HIV test may have identified signs or symptoms of
disease and actively sought an HIV test. Those who tested at the mobile may have taken the
immediate opportunity to test that a mobile service offers [
] and may not have been aware
of any signs or symptoms of disease. The presumption that clients diagnosed at mobile were
not driven to test due to their own awareness of symptoms may have delayed them linking to
care. Studies have shown that individuals who are feeling ªwellº i.e. have higher CD4 counts
], are asymptomatic [
], have no TB symptoms [
] are less likely to link to HIV care.
Future research is required to investigate factors associated with linkage to care from
community-based services to provide an empirical basis for designing interventions aimed at
improving linkage to care, in particular from mobile HTS.
Sex, age and TB co-infection were not associated with linkage to HIV care. This concurs
with a Cape Town study that showed age and sex did not predict linkage to care for individuals
who self-initiated an HIV test at public health facilities [
], but differs from another study
that found older individuals were more likely to link to care from home-based services [
Overall, the majority of clients diagnosed with TB linked to treatment. This finding is
higher than what was reported in another Cape Town study where 57% of individuals
diagnosed with TB, linked to care from a mobile service [
]. Our finding is similar to that found
in individuals diagnosed with TB at public health facilities [
]. Although the majority of
clients diagnosed with pulmonary TB in our study linked to Tb treatment, almost a quarter did
not. This has serious public health implications as these individuals continue to spread TB in
In our study, of clients diagnosed with TB, 76.4% linked to TB treatment compared to
63.1% of HIV-infected clients who linked to HIV care. We hypothesise that; (i) there were a
smaller number of clients diagnosed with TB (275) compared to the number diagnosed with
HIV (5 929) and healthcare workers may have found this more manageable, (ii) as pulmonary
TB is infectious, healthcare workers may have made more of an effort to link these clients to
care, or (iii) TB treatment was available to everyone diagnosed with TB whereas antiretroviral
therapy was only available to individuals who met the eligibility criteria at the time. As
pointof-care CD4 testing was not done in this study, clients would have been unaware of their
eligibility for ART until they linked to HIV care. Further research is needed to test these
assumptions to better understand how linkage to care and treatment may be different for those
diagnosed with HIV and TB.
Linkage to TB treatment was associated with age. Compared to clients aged 12±24 years,
clients in older age groups were less likely to link to TB treatment. Younger clients may have
been easier to follow up, especially if they were still in school or this may have been their first
TB episode and they may have been more motivated to link to treatment than older clients,
who may have experienced previous TB treatment. More research is needed to better
understand the association between age and linkage to TB treatment. Sex, HIV testing service and
HIV co-infection were not associated with linkage to TB treatment. There is a lack of literature
around factors associated with linkage to TB treatment from community-based HTS and more
work is needed in this area.
In order to reach the `90-90-90' goals and bring the dual TB and HIV epidemics under
control, improved linkage to care and treatment is essential. Although our study showed higher
rates of linkage to care compared to other studies from Cape Town, these remain suboptimal.
In our study setting, general messaging supported TB as a curable disease [
] and HIV as
a lifelong chronic disease [
] and TB and HIV care and treatment was freely available from a
multitude of primary health care facilities. We therefore speculate that other factors, apart
from promoting the benefits of treatment and having treatment services available free of
charge, are associated with linkage to care and treatment. Community-based services could
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consider establishing an effective referral network, accompanying the patient to the health
] and providing on-going follow-up to improve linkage to HIV care and treatment.
ART is currently available for all people living with HIV in South Africa, irrespective of
CD4 count (universal test and treat (UTT)) [
]. We speculate that linkage to HIV care will
not necessarily improve as UTT is rolled out. We hypothesise that initial awareness of signs or
symptoms of disease may play a larger role in linkage to care and treatment than demographic
(e.g. sex and age), clinical (e.g. diagnosed disease or co-infection) or health service factors
(referral letter). Future studies should determine the impact of UTT on linkage to care from
A major strength of this study is that it incorporates a large number of client records that
were routinely collected from community-based HTS modalities (8 stand-alone centres and 8
mobile services), implemented locally, to generate knowledge around linkage to HIV care and
TB treatment. This study adds to the limited body of literature that describes integration of TB
services into community-based HIV testing and linkage to care and treatment from
community-based HTS in South Africa. Previous research has focused on linkage within HIV or TB
services, but not an integrated service. Secondly, this study identified the need for specific
linkage to HIV care interventions from mobile HTS.
The main limitation is that linkage to care and treatment was self-reported. It was not
possible to confirm linkage to care against health facility records. Acknowledging that it takes time
for clients to come to terms with an HIV positive diagnosis, some clients may have linked to
care after the 3-month period. Potentially, linkage to care reported in this study may be
underestimated, but balanced by over-reporting of socially desirable answers given over the phone
by clients. Secondly, the routine data for this study was collected during a period when
eligibility criteria for ART were based on a CD4 threshold. No data on CD4 count was collected and
therefore it was not possible to determine linkage to care trends over the study period
according to eligibility criteria of new guidelines. Future studies should evaluate linkage to care trends
over time and the influence of eligibility criteria. Thirdly, only a few variables were available to
be evaluated because the study used routinely collected data. This makes the study limited in
terms of its findings. In addition, the results are only generalizable to similar peri-urban areas;
future research should determine factors associated with linkage to care for community-based
services in rural settings.
In order to reach the `90-90-90' target and control dual HIV and TB epidemics in South Africa,
improved linkage to care is vital. A large proportion of clients diagnosed with HIV at mobile
services did not link to care and almost a quarter of clients diagnosed with TB did not link to
treatment. Integrated community-based HIIV testing services can diagnose HIV and TB, but
improved linkage to care strategies are vital. Future studies should investigate interventions
that provide extended client support to facilitate improved linkage to care in similar HIV and
TB high-burden settings for improved impact on public health.
S1 Table. Factors associated with linkage to HIV care and TB treatment among adolescents
and adults between 2008 and 2012 in the Cape Town Metropolitan district, South Africa,
by HIV testing service.
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Conceptualization: Sue-Ann Meehan, Pren Naidoo, Ronelle Burger, Nulda Beyers.
Data curation: Sue-Ann Meehan.
Formal analysis: Sue-Ann Meehan, Rosa Sloot, Heather R. Draper.
Funding acquisition: Sue-Ann Meehan.
Investigation: Heather R. Draper, Nulda Beyers.
Methodology: Sue-Ann Meehan, Rosa Sloot, Heather R. Draper, Pren Naidoo, Ronelle Burger,
Project administration: Sue-Ann Meehan, Pren Naidoo.
Supervision: Ronelle Burger, Nulda Beyers.
Writing ± original draft: Sue-Ann Meehan.
Writing ± review & editing: Sue-Ann Meehan, Rosa Sloot, Heather R. Draper, Pren Naidoo,
Ronelle Burger, Nulda Beyers.
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