WHO HIV 2013.82 Eng

WHO/HIV/2013.
82 © World Health Organization 2013
Title: Integration of HIV and TB services:

• a: Does ART provided at the TB clinic result in better outcomes than referring people with
TB and HIV for ART in specialized HIV clinics?
• b: Does TB diagnosis and/or TB treatment at specialized HIV clinics result in better
outcomes than referring people living with HIV to TB clinics for TB diagnosis and/or TB
treatment?
Contents
1. PICO question ....................................................................................................................................... 1
2. Search strategy ...................................................................................................................................... 2
3. Flow diagram of screening process ....................................................................................................... 3
4. Evidence summaries ............................................................................................................................. 3
4.1. Observational studies ........................................................................................................................ 3
5. Quality of evidence ............................................................................................................................... 9
5.1. PICO a: Does ART provided with TB treatment at the TB clinic result in better outcomes than
referring people with TB and HIV for ART in specialized HIV clinics? ..................................................... 9
5.2. PICO b: Does TB diagnosis and/or TB treatment at specialized HIV clinics result in better
outcomes than referring people living with HIV to TB clinics for TB diagnosis and/or TB treatment? .... 10
6. Bibliography of included studies ........................................................................................................ 10
7. Excluded studies with reasons ............................................................................................................ 15
1. PICO questions
a Provision of HIV treatment and care at TB clinics

P People in countries with a high burden of TB and HIV coinfection
I ART and HIV care services provided with TB diagnosis and treatment at the TB clinics
C Provision of ART and HIV care services separately from TB diagnosis and treatment
O HIV incidence, transmission, mortality, morbidity, access, retention and other outcomes to be noted
in the protocol
b Provision of TB treatment and care at HIV clinics

P People in countries with a high burden of TB and HIV coinfection
I TB diagnosis and treatment at HIV care clinics
C Referral of PLHIV to TB clinics for diagnosis and treatment of TB
O HIV incidence, transmission, mortality, morbidity, access, retention, and other outcomes to be
noted in the protocol
This work was commissioned by the World Health Organization and carried out by The University of California, San
Francisco (UCSF), Cochrane Review Group on HIV/AIDS
1
WHO/HIV/2013.82 © World Health Organization 2013
2. Search strategy
2
3. Flow diagram of screening process
Records after duplicates

removed Citations excluded based
(n = 461) on details in abstracts
(n = 442)
Additional records Full-text articles assessed Full-text articles excluded

identified through for eligibility (n = 20)
cross-referencing (n = 19) + 11 (identified
other sources from cross-references)
(n = 10) = 29
Additional
conference abstracts
identified Studies included
(n = 13) (all (abstracts and full-
included) text articles)
(n = 23)
4. Evidence summaries
4.1. Observational studies
4.1.1. ART provided at the TB clinic (where TB treatment is also provided) compared to
referring people with TB and HIV for ART in specialized HIV clinics [PICO a]
Outcome: ART uptake “after” the TB clinic began providing ART (versus “before”). See Fig. 2 and
3. Twelve before-and-after studies show increased uptake after ART is started to be provided in TB
clinics. The evidence was downgraded due to possible confounding by other interventions and events
(such as changes in ART initiation criteria) during the study time frame. One study (Kerschberger 2012)
adjusted for other factors influencing ART initiation, such as CD4 count. The study by van Rie (2008)
directly addresses the comparison of interest. Two studies (Bygrave 2010, Kerschberger 2012) describe a
variation on the intervention; instead of the TB clinic providing ART, a one-stop shop1 provides both TB
and HIV diagnosis and treatment. In several studies, imprecision is an issue due to small numbers of
patients with events. All but one (Bygrave 2010) of these studies report increase in ART uptake after the
TB clinic began providing ART. Very low quality evidence from
1
Médecins Sans Frontières (MSF), the technical partner in the Kerschberger et al. (2012) and Bygrave et al. (2010)
studies, defines one-stop shops as clinics in which people with HIV and TB visit one clinician on the same day, in
the same room, with a single patient chart and drug delivery point.
3
• One study (van Rie 2008) in the Democratic Republic of the Congo found higher proportions of
people with TB and HIV initiating ART after TB clinics began providing ART, compared with
before, when people with TB and HIV were referred to an ART centre (RR 2.86, 95% CI 2.06–
3.97).
• Two studies (Pevzner 2011, Howard 2012) using national surveillance data found higher
proportions of people with TB and HIV receiving ART2 in the years after TB clinics began to
provide ART, compared to before this service delivery change. Pevzner et al. (2011) (Rwanda)
found a RR of 4.84 (95% CI 4.34–5.41) comparing years after TB clinics began providing ART
to before this service delivery change. Howard (2012) (Kenya) found a RR of 1.59 (95% CI 1.56–
1.62) comparing a similar change in service delivery.
• In one study (Kerschberger 2012), people with TB and HIV attending a nurse-run one-stop shop
in South Africa were two times more likely to initiate ART (adjusted HR 1.6, 95% CI 1.11–2.29)
compared to those attending the same primary care clinic in the year before when they were
referred to an ART clinic in a separate facility.
• In one study (Bygrave, 2010), nurse-managed “one-stop shops” were established in rural primary
health care clinics in Lesotho; before then, people with TB and HIV were referred to a district
hospital for ART (and to initiate TB treatment). The proportion of eligible patients receiving ART
two years after the “one-stop shops” were introduced was significantly decreased when compared
to one year after this was introduced (RR 0.89, 95% CI 0.81–0.98).
• One study (Morse 2012) in Zambia found a higher proportion of people with TB and HIV
initiating ART after the TB clinics in two primary health centres began to provide ART compared
to historical controls when patients were referred to a separate HIV clinic in the same health
facilities (RR 2.27, 95% CI 1.45–3.56).
• Two studies (Chifundo 2010, Huerga 2010) found higher proportions of people with TB and HIV
receiving ART after the TB clinic in a district hospital began providing ART compared to before
when people with TB were referred to the separate HIV clinic within the same district hospital.
Chifundo (2010) (Malawi) found an RR of 1.72 (95% CI 1.54–1.94) when comparing one year
after the TB clinic began providing ART to the year the intervention was introduced. Huerga
(2010) (Kenya) found an RR of 5.40 (95% CI 3.37–7.94) when comparing the year after to the
year before the intervention was introduced.
• One study (Phiri 2011) in Malawi found higher proportions of people with TB and HIV receiving
ART during the first year when TB clinic began to provide ART, compared to the year before
when their patients were referred within the same facility to the HIV clinicians to initiate ART
(RR 1.16, 95% CI 1.09–1.23).
• In one study (Mugo, 2009) in Kenya, the proportion of people with TB enrolled on ART
increased 45% after the TB clinic in the district hospital began to provide ART, but no
denominators were available to make any statistical inference.
• One study (Odhiambo 2012) in Kenya found an increase in the percentage of people with TB
receiving ART after the province implemented ranges of service integration models, but no
denominators were available to make any statistical inference. (These data are presumably
included in the national surveillance data in Howard (2011).)
• One study (Kambale, 2010) in the Democratic Republic of the Congo found that the number of
people with TB receiving ART increased after TB clinics began providing ART, but
denominators are not specified.
2
At any time before TB treatment is completed, whether ART naive or already receiving ART at the time of TB
diagnosis.
4
Outcome: ART uptake when provided by an HIV clinic collocated with the TB clinic (versus
referral to a geographically separated HIV clinic). See Fig. 3. The quality of evidence in these studies
is very low for several reasons. These are more indirect than the studies above; both the collocated and
the geographically separated models required people with TB to be referred to specialized HIV clinics. In
fact, the intervention model in these studies is used as the comparison in six of the studies listed above
(Chifundo, Huerga, Morse, Mugo, Phiri and Kerschberger). In contrast to the before-and-after studies, the
comparisons in these studies are made during the same calendar period so they are less subject to events
over time. However, there is a risk of bias in the studies that did not adjust for other factors influencing
ART uptake (such as CD4 count) or service enhancements in the intervention (besides the co-location of
HIV and TB clinics). Imprecision is an issue in several of the studies. The results of these four studies are
inconsistent; two found that ART uptake improved, but two found no statistically significant differences
in ART uptake.
• In one study (Louwagie 2012) in South Africa, eligible people with TB attending a facility with
collocated TB and HIV clinics were more than twice as likely to start ART during TB treatment
than patients referred to start ART in geographically separated HIV clinics (subhazard ratio 2.49,
95% CI 1.06–5.88).
• In one study (Muvuma 2012) in Zambia, ART uptake was higher in people with TB and HIV
attending health facilities with visiting (mobile) ART services than in those referred to start ART
during treatment in geographically separated HIV clinics during the same time period (OR 8.82,
95% CI 0.56–138), although this estimate is not significant with a very wide confidence interval.
• One study (Schwartz, 2012) in Botswana found that patients of TB clinics with collocated HIV
clinics were no more likely to initiate ART during TB treatment than patients from clinics
without collocated HIV clinics (RR 0.95, 95% CI 0.75–1.20). (This comparison is calculated for
this review based only on patients with ART initiation data.)
• One study (Ikeda, 2012) compared ART uptake in people with TB newly diagnosed with HIV in
a regional TB hospital in Guatemala after an ART clinic was added versus before, when people
with TB and HIV were referred elsewhere for ART. The proportion starting ART was
significantly higher once ART was available on site (OR 9.62, 95% CI 5.26–17.57). (The time
frame for ART initiation relative to TB treatment is not specified.)
Outcome: timeliness of ART initiation among people who began ART during TB treatment. See Fig.
3 and 4.
• In one study (Phiri 2011), during the first year TB officers in an HIV and TB clinic in Malawi
began to provide ART, people with TB and HIV were more likely to start ART during the first
two months of TB treatment compared to before when people with TB were referred down the
hall to HIV care clinic (RR 2.22, 95% CI 1.93 to 2.56).
• One study (Schwartz 2012), there was no difference in the proportion starting ART within 60
days of TB treatment initiation, when patients started TB treatment in facilities with collocated
HIV clinics were compared to those referred for ART in geographically separate HIV clinics (RR
0.83, 95% CI 0.56 to 1.24). Since baseline CD4 count was associated with time to ART initiation,
authors also looked at median time to ART initiation in those with CD4 counts of 100 cells/mm3
or less, and found no difference by clinic type.
• In one study (Lawn 2011) in South Africa, patients with CD4 counts lower than 50 cells/mm3
starting TB treatment in an ART clinic were more likely to start ART within four weeks after TB
treatment initiation than patients referred from TB clinics (RR 4.91, 95% CI 1.98 to 12.2 for the
5
most recent calendar period). In a competing risk regression analysis, the time from TB diagnosis
to start of ART was substantially shorter for patients with TB diagnosed in the ART clinics,
compared to patients referred from TB clinics (adjusted sub-hazard ratio 0.53, 95% CI 0.43 to
0.66).3
Outcome: referral or enrolment into HIV care. See Fig. 3. The two studies that reported on these
process indicators provide very low quality evidence due to study bias and indirectness. In addition,
Morse has very few cases (imprecision).
• One study (Louwagie 2012) in South Africa, eligible people with TB attending a facility with
collocated TB and HIV clinics were more likely to be referred for HIV-related care than in
geographically separated HIV clinics (RR 2.75, 95% CI 2.28–3.32).
• One study (Morse 2012) in Zambia found a higher proportion of people with TB and HIV
enrolling in HIV care after the TB clinics in two primary health care centres began to provide
ART, compared to historical controls, when patients were referred to a separate HIV clinic in the
same health centres (RR 1.65, 95% CI 1.18–2.32).
Outcome: mortality. See Fig. 2 and 3. The quality of evidence is very low and was downgraded for
imprecision (few patients), indirectness (only van Rie (2008) reports the same intervention and
comparator as the PICO question), and study limitations including differential follow up, and no
adjustment for confounders (van Rie 2008, Ikeda 2012). Given these differences, it is not surprising that
the three studies found inconsistent results.
• One study (Schwartz 2012) in Botswana found no significant difference in mortality during TB
treatment among people with HIV and TB with CD4 counts ≤250 cell/mm3 who started outpatient
TB treatment in TB clinics with or without collocated HIV clinics (RR 1.27, 95% CI 0.58–2.76).
• One study (van Rie 2008) in the Democratic Republic of the Congo found a lower proportion of
people living with HIV died during TB treatment compared to the people with TB and HIV
registered before the clinics began providing ART (RR 0.36, 95% CI 0.17–0.77).
• One study (Ikeda 2012) evaluated the impact of adding an ART clinic to a regional TB hospital in
Guatemala. Compared to before, when people with TB and HIV were referred elsewhere for ART,
the OR for death at 50 weeks of follow up was 0.08 (95% CI 0.05–0.15).
Outcomes during TB treatment: TB treatment success.4 See Fig. 2 and 3. Two studies report only one
TB treatment outcome (success) provide very-low-quality evidence due to indirectness of the comparator
and/or intervention model and the lack of adjustment for other factors affecting mortality among people
living with HIV (such as ART and baseline CD4 count) or other interventions during the study period that
were likely to have contributed to improved outcomes.
• In one study (Bygrave, 2010) in Lesotho, the proportion with TB treatment success was not
significantly higher in the cohort of people with TB and HIV registered two years after the
3
Reciprocal of the published article, since this systematic review compares patients starting TB treatment in the
HIV clinic to those referred from TB clinics.
4
TB treatment success includes patients with documented cure (acid-fast bacilli smear-negative sputum) and
patients completing their course of treatment without documentation of cure.
6
creation of a one-stop shop compared to one year after (RR 1.08, 95% CI 0.96–1.21).
• In one study (Huerga 2010), the proportion with TB treatment success was not significantly
higher in the cohort of patients receiving ART starting TB treatment four to five years after the
TB clinic began to provide ART compared to the cohort starting TB treatment (and ART) two
years after (RR 0.93, 95% CI 0.83–1.03). Similarly, there was no difference in TB treatment
success among people with TB and HIV not receiving ART (RR 1.06, 95% CI 0.88–1.27).
All TB treatment outcomes. See Fig. 3. The two studies that reported on TB treatment outcomes provide
very-low-quality evidence due to indirectness, lack of adjustment for confounders such as receiving ART
(Kaplan 2012) or CD4 count at ART initiation (Dube 2010) and imprecision.
• In one study (Kaplan 2012),5 people with TB and HIV registered in facilities providing both TB
and ART were less likely to achieve TB treatment success when compared to patients who were
referred off site for ART (RR of TB treatment success 0.90, 95% CI 0.88–0.92). There was no
difference in TB treatment failure for people with TB and HIV registered in facilities providing
both TB treatment and ART compared to those providing TB treatment with ART offsite (RR of
TB treatment failure 1.15, 95% CI 0.79–1.67). Further, patients in facilities providing both TB
treatment and ART were more likely to die or default from TB treatment than patients referred off
site for ART (RR of death 1.26, 95% CI 1.04–1.52; RR of defaulting 1.19, 95% CI 1.02–1.39).
• One study (Dube 2010) found no differences in TB treatment outcomes for patients receiving
ART after mobile ART services were provided on site, compared to before, when patients were
referred off site to receive ART (RR for treatment success 1.21, 95% CI 0.98–1.51; RR for TB
treatment failure or death 0.38, 95% CI 0.13–1.07; RR for defaulting 0.61, 95% CI 0.90–4.12).
4.1.2 TB diagnosis and/or treatment at HIV clinics compared to referring people living with HIV
to TB clinics for TB diagnosis and/or TB treatment [PICO b]
Outcome: proportion of people living with HIV screened for TB. See Fig. 6.
• One study (Howard 2009) in six African countries found that the proportion of people living with
HIV screened for TB using a symptom questionnaire was higher in HIV facilities with TB
treatment on site than in HIV sites that had to refer for TB treatment off site (RR 1.36, 95% CI
1.32–1.40). The evidence is very low quality due to risk of bias (weighted proportions were used
to calculate the proportion screened for TB).
Outcome: ART uptake. See Fig. 7.
This evidence is very low quality due to imprecision and possible confounding by other interventions
during the study periods that accompanied the reorganization of services. This study also provides
indirect evidence, since the comparisons are different from the PICO question.
• One study (Hermans 2012) in Uganda found a lower proportion of people with TB and HIV
starting ART one year after the creation of a TB and HIV unit within the HIV service compared
to before when people with TB were referred to a discrete TB clinic (also within the HIV service)
5
One of this study’s 13 facilities providing both TB treatment and ART is the same clinic described in Brown
(2011).
7
(RR 0.86, 95% CI 0.75–0.99). The authors attribute this decrease to clinicians appropriately
giving priority to patients with lower CD4 counts when faced with an ART shortage. Patients
with CD4 counts ≥250 cells/mm3 were less likely to receive ART after the creation of a TB and
HIV unit compared to before (RR 0.40, 95% CI 0.21–0.76).
Outcome: timeliness of ART initiation. See Fig. 7.
• One study (Hermans 2012) in Uganda found that a higher proportion of people with TB and HIV
started ART during the intensive phase of TB treatment among those starting TB treatment one
year after a TB and HIV unit was created within the HIV service compared to before when people
with TB were referred to a discrete TB clinic (RR 2.62, 95% CI 1.90–3.58). This evidence is
downgraded for imprecision, indirectness as well as possible confounding (including providers
learning during the study period of new evidence supporting earlier ART).
Outcomes of TB treatment. See Fig. 7 and 8. This is very-low-quality evidence. Since the intervention
in Bento (2010) and Cerda (2011) are home care models, these provide indirect evidence. Evidence was
also downgraded for possible confounding (directly observed therapy in Bento (2010)), by other
interventions during the study period (all three studies) and differential ascertainment of death (Hermans
2012).
• In one study (Hermans 2012) in Uganda, one year after the creation of a TB and HIV unit within
the HIV service, there was no difference in TB treatment success for people living with HIV
started on ART (RR 1.04, 95% CI 0.92–1.17) and no difference in death or loss to follow-up (RR
0.83, 95% CI 0.49–1.38) compared to before when people with TB were referred to a discrete TB
clinic (also within the HIV service). By contrast, these outcomes improved for people with TB
not receiving ART after the creation of the TB and HIV unit compared to before when they were
referred to a discrete TB clinic (RR for treatment success 1.59, 95% CI 1.07–2.36; RR for death
or loss to follow up 0.65, 95% CI 0.49-0.87)
• One study (Bento 2010) in Brazil found no difference in TB treatment success (RR 1.03, 95% CI
0.81–1.30) and lower defaulting (RR 0.42, 95% CI 0.24–0.76) but increased mortality (RR 3.33,
95% CI 0.98–11.37) among people with TB and HIV receiving weekly home visits (delivering
TB medicines and ART for administration by a caregiver) compared to patients who picked up
their TB medicines and ART from a hospital outpatient department for self-administration.
• In one study (Cerda 2011) in Peru, patients receiving directly observed TB treatment and
supervised ART at home had a lower hazard of dying or defaulting from treatment (adjusted HR
0.34, 95% CI 0.12–0.98) than people with TB and HIV referred to district health centres for
directly observed TB treatment. Patients receiving directly observed TB treatment and supervised
ART at home had a nonsignificant increase in likelihood to achieve cure (adjusted RR 1.28, 95%
CI 0.90–1.83) than people with TB and HIV referred to district health centres for directly
observed TB treatment.
Outcomes: resource utilization. See Fig. 8.
• In one study (Cerda 2011) in Peru, patients receiving directly observed TB treatment and
supervised ART at home used fewer total hospital days per person per year of observation than
people with TB and HIV referred to district health centres for directly observed TB treatment
(adjusted incidence rate ratio 0.37, 95% CI 0.14–0.99). This study provides very-low-quality
evidence due to indirectness and confounding by other interventions implemented along with the
home delivery model.
8
5. Quality of evidence
5.1. PICO a: Does ART provided with TB treatment at the TB clinic result in better outcomes than
referring people with TB and HIV for ART in specialized HIV clinics?
For ART uptake, the quality of the evidence is very low. The most direct evidence comes from the 11
studies comparing ART uptake after versus before ART began being provided by TB clinics (Fig. 2, top
of Fig. 3). However, only Kerschberger et al. (2012) adjusted for other patient factors influencing ART
initiation (such as CD4 count). In most studies, the change in service delivery was one part of a package
of additional interventions to improve TB and HIV service coordination. There was also possible
confounding by events during the study period, such as the release of new guidelines to initiate ART
sooner after TB treatment initiation and among patients with higher CD4 counts. Several studies had
small numbers of patients, leading to imprecise measurements. This group of studies reports fairly
consistent increases in ART uptake after the TB clinic began providing ART.
The three studies comparing collocated clinics to geographically separate clinics (bottom of Fig. 3) during
one period (Louwagie 2012, Muvuma 2012, Schwartz 2012) avoid the problem of confounding by events
over calendar time and also adjusted for several confounders. However, the evidence from these studies is
less direct, since both the collocated and geographically separated clinics require people with TB to be
referred to specialized HIV clinics (Fig. 3). The results of these three studies are less consistent; only
Louwagie (2012) found a statistically significant improvement in ART uptake. Ikeda (2012) also
compared ART uptake in collocated versus geographically separate clinics but used an after versus before
design without adjustment for confounding by calendar events, other interventions during the time frame
or patient characteristics.
For timeliness of ART initiation, the quality of the evidence is very low. The three relevant studies do not
directly address the question; the intervention was referral to a collocated HIV clinic (Schwartz 2012) or
an HIV clinic providing TB treatment (Lawn 2011), and the comparator was referral within the same
facility (Phiri 2011). Given three different comparisons (Fig. 3, 4), inconsistent results would be expected.
Two of the three studies found higher proportions of people with TB and HIV initiating ART within the
first one to two months, but Schwartz (2012) found no difference.
For TB treatment outcomes, the quality of the evidence is very low. Three studies (Schwartz (2012), van
Rie (2008) and Ikeda (2012)) reported mortality in people with TB and HIV (without information on
other TB treatment outcomes). The evidence was downgraded for imprecision (few patients), indirectness
(only van Rie (2008) reports the same intervention and comparator as the PICO question), and study
limitations including differential follow-up, and no adjustment for confounders (van Rie 2008, Ikeda
2012). Given these differences, inconsistent results would be expected.
Two studies reported no significant change in TB treatment success (Bygrave 2010, Huerga 2010). The
quality of evidence is very low due to indirectness and the lack of adjustment for other factors affecting
mortality among people living with HIV (such as ART and CD4 count) or other interventions during the
study period that were likely to have contributed to improved outcomes.
The two studies that reported on all TB treatment outcomes provide very low quality of evidence due to
indirectness, lack of adjustment for confounders such as receiving ART (Kaplan 2012) or CD4 count
(Dube 2010) and imprecision.
9
We found no studies that explored such outcomes as viral suppression, immune recovery, immune
reconstitution inflammatory syndrome, adverse events or retention on ART during or after TB treatment.
5.2. PICO b: Does TB diagnosis and/or TB treatment at specialized HIV clinics result in better
outcomes than referring people living with HIV to TB clinics for TB diagnosis and/or TB
treatment?
For TB screening, the quality of the evidence is very low due to risk of bias.
For ART uptake and the timeliness of ART initiation, the quality of the evidence is also very low due to
imprecision, indirectness and possible confounding by other interventions during the study periods that
accompanied the reorganization of services.
For TB treatment outcomes among people living with HIV, the quality of the evidence was downgraded
to very low for indirectness, confounding by other interventions and differential ascertainment of death.
The evidence for resource utilization was also very low quality, due to indirectness and confounding by
other interventions.
We found no studies that reported outcomes of viral suppression, immune recovery, retention in ART or
timeliness of TB diagnosis.
6. Figures
Fig 1. Does ART provided with TB treatment at the TB clinic result in better outcomes than referring
HIV-infected TB patients for ART in specialized HIV clinics?
HIV TB
TB
Provides ART Refers for ART
Fig 2. After versus before
10
TB
Provides ART
Kambale,* Pevzner, Howard, van

HIV TB
Rie
* “before” model not specified
Refers for ART

TB/HIV
Same nurse provides

TB treatment and ART
Kerschberger, Bygrave,Odhiambo**
**A few % of settings used “partially integrated” or
“collocated” models.
Fig 3. After versus before
HIV TB
HIV TB
TB staff provides ART Refers for ART
Chifundo, Huerga, Morse, Mugo, Phiri
Fig 4. ART initiation among people who began ART during TB treatment
11
HIV-infected patients in care at HIV HIV-infected TB patients referred from TB

clinic; found to have TB; start ART and Clinics to specialized HIV clinic to start ART
TB treatment
TB
HIV
TB
Referrals for ART
Lawn
Fig 5. Does TB diagnosis and / or TB treatment at specialized HIV clinics result in better outcomes than
referring HIV-infected patients to TB clinics for TB diagnosis and/or treatment?
HIV TB
HIV
Treat and/or diagnose TB Refer for TB treatment and/or diagnosis
Fig 6. 159 HIV sites versus 22 HIV sites that refer that treat TB
12
HIV TB
HIV
Treat TB
Refer for TB treatment
Howard, 2009
Fig 7. After creation of TB / HIV unit versus before
HIV
HIV
TB/HIV
TB
Refers for TB treatment
Hermans
Fig 8. HIV team visits patient’s home to provide TB treatment versus patient travels to TB clinic for TB
treatment
13
TB
Bento,* Cerda
*organization of TB and HIV services in outpatient department is not specified
7. Bibliography of included studies
Peer-reviewed articles
1. Bento C, Pedroso E. Assessment of the effectiveness of a home-based care program for patients
coinfected with tuberculosis and human immunodeficiency virus after discharge from a reference
hospital in south-eastern Brazil. Braz J Infect Dis 2010; 14(6): 594-600.
2. Cerda R, Munoz M, Zeladita J, Wong M, Sebastian JL, Bonilla C, Bayona J, Sanchez E, Arevalo J,
Caldas A, Shin S. Health care utilization and costs of a support program for patients living with the
human immunodeficiency virus and tuberculosis in Peru. Int J Tuberc Lung Dis 2011; 15: 363-368.
3. Hermans SM, Castelnuovo B, Katabira C, Mbidde P, Lange JM, Hoepelman AI, Coutinho A, Manabe
YC. Integration of HIV and TB services results in improved TB treatment outcomes and earlier
prioritized ART initiation in a large urban HIV clinic in Uganda. J Acquir Immune Defic Syndr 2012;
60: e29-35.
4. Howard A, Gasana M, Getahun H, Harries A, Lawn S, Miller B, Nelson L, Sitienei J, Coggin W.
PEPFAR support for the scaling up of collaborative TB/HIV activities. JAIDS 2012; 60(3): S136-
144.
5. Huerga H, Spillane H, Guerrero W, Odongo A, Varaine F. Impact of introducing human
immunodeficiency virus testing, treatment and care in a tuberculosis clinic in rural Kenya. Int J
Tuberc Lung Dis 2010; 14(5): 611-15.
6. Kerschberger B, Hilderbrand K, Boulle A, Coetzee D, Goemaere E, De Azevedo V, Van Cutsem G.
The effect of complete integration of HIV and TB services on time to initiation of antiretroviral
therapy: a before-after study. PLoS ONE 2012; 7(10):e46988.
7. Lawn SD, Campbell L, Kaplan R, Little F, Morrow C, Wood R. Delays in starting antiretroviral
therapy in patients with HIV-associated tuberculosis accessing non-integrated clinical services in a
South African township. BMC Infectious Diseases 2011; 11:258.
8. Louwagie G, Girdler-Brown B, Odendall R, Rossouw T, Johnson S, Van der Walt M. Missed
opportunities for accessing HIV care among Tshwane tuberculosis patients under different models of
care. Int J Tuberc Lung Dis 2012; 16(8): 1052-58.
14
9. Pevzner E, Vandebriel G, Lowrance D, Gasana M, Finaly A. Evaluation of the rapid scale-up of

collaborative TB/HIV activities in TB facilities in Rwanda, 2005-2009. BMC Public Health 2011;
11:550.
10. Phiri S, Khan PY, Grant AD, Gareta D, Tweya H, Kalulu M, Chaweza T, Mbetewa L, Kanyerere H,
Weigel R, Feldacker C. Integrated tuberculosis and HIV care in a resource-limited setting: experience
from the Martin Preuss centre, Malawi. Trop Med Int Health 2011; 16:1397–403.
Conference abstracts
1. Bygrave H, Trivino L, Makakole L. TB/HIV integration: lessons learned from implementation of a

TB/HIV “one stop shop” at primary health care clinics in rural Lesotho. AIDS 2010 – XVIII
International AIDS Conference: Abstract no. MOAB0301.
2. Chifundo K, Wandwalo E, Kanyerere H, et al. What is the best model of TB/HIV service delivery?
Experience from Malawi. AIDS 2010 – XVIII International AIDS Conference: Abstract
no. MOPE0858.
3. Dube C, Kayama N, Miyano S, et al. Step forward to health system strengthening: the impact of
scaling up of ART services on TB services in rural settings, Zambia. AIDS 2010 – XVIII
International AIDS Conference: Abstract no. THAE0104.
4. Howard AA, Saito S, Nash D, Flam R, Elul B, Scardigli A, Oyeledun B, Cunningham A, Hoos D,
and El-Sadr W. On-Site location of TB services is associated with TB screening of HIV-infected
patients at enrollment in HIV care programs in 6 sub-Saharan African countries. 2009 CROI. #590.
5. Ikeda J, Page K, Hudes E, Barrios R, López Tellez CA, Hearst N. HIV and TB and Integration
reduces mortality among the indigenous population in rural Guatemala. AIDS 2012.
6. Kambale A, Okiata JP, Okenge A, et al. Impact of the expansion of NTP-based HIV care on TB
outcomes in DR Congo. UNION. 2010. PS-100688-14.
7. Kaplan R, Caldwell J, Bekker L-G, Jennings K, Lombard C, Enarson D, Beyers N, Wood R.
Provision of ART in TB facilities in Cape Town South Africa: impact on TB treatment outcomes.
UNION. 2012. Abstract # OP-147-16.
8. Morse J, Luhanga D, Harris J, Musople R, Besa S, Nhandu V, Samungole G, Kancheya N. Integrated
TB/ART clinics in Lusaka, Zambia: an evaluation of enrollment into HIV care and early initiation of
antiretroviral therapy in TB/HIV co-infected patients. UNION. 2012. Abstract #PC-545-17.
9. Mugo P, Gachengo J, Muguongo R, et al. Integrating TB and HIV care services: experience from a
rural district hospital in Kenya. UNION. 2009. PS-94524-07.
10. Muvuma S, Miyano S, Ishikawa N, Sikaze I, Moyo C, Kapyata H, Changala M, Msiska C, Syakantu
G. Poor linkages between TB and HIV services affects the quality of care; a retrospective cohort
study of TB/HIV patients from HIV testing to ART initiation in a rural setting in Zambia. AIDS
2012.
11. Odhiambo J, Gondi J, Miruka F, Muttai H, Cain K, Ochanda B, Sitienei JK, Nganga L, Soti D.
Models of TB-HIV integration and accomplishments in Nyanza Province, Kenya. UNION 2012. PC-
542-17.
12. Schwartz A, Tamuhia N, Steenhoff A, Nkakana K, Letlhogile R, Chadborn T, and Bisson G.
Outcomes among HIV+ adults with active pulmonary TB treated in clinics with and without on-site
HIV clinics—a retrospective cohort study: Botswana. 2012 CROI. #928.
13. Van Rie A, Roger I, Edmonds A, et al. Implementation of primary health care ART model for HIV
co-infected TB patients improves treatment outcomes. UNION. 2008. TS-82281-19.
8. Excluded studies with reasons
Reference Reason for exclusion

15
(missing element population,

intervention, comparator)
Abdool Karim SS, Naidoo K, Grobler A, Padayatchi N, Baxter C, No comparison for site of ART.
Gray A, Gengiah T, Nair G, Bamber S, Singh A, Khan M, Pienaar J, (C)
El-Sadr W, Friedland G, Abdool Karim Q. Timing of initiation of
antiretroviral drugs during tuberculosis therapy. N Engl J Med 2010;
362: 697-706.
Atkins S, Lewin S, Jordaan E, Thorson A. Lay health worker- No description of HIV status or
supported tuberculosis treatment adherence in South Africa: an ART. (P, I)
interrupted time-series study. Int J Tuberc Lung Dis 2011; 15:1, 84-
89, i.
Beversluis D, Musoke R, Mandima P, Nyamapfeni P, Chipato T, No details of where TB diagnosis
Mukasa JB, Byamugisha J, Mugerwa R, Morrison C, Salata RA. and/or treatment were provided
Incidence of major clinical outcomes in a cohort of Ugandan and in either country. (I, C)
Zimbabwean women with HIV-1 infection followed from
seroconversion. International Journal of STD and AIDS 2012; 23:
111-114.
Bonnet MMB, Pinoges LLP, Varaine FFV, Oberhauser BBO, No comparison of TB diagnosis
O’Brien DDO, Kebede YYK, Hewison CCH, Zachariah RRZ, and/or treatment in HIV clinic
Ferradini LLF. Tuberculosis after HAART initiation in HIV-positive versus TB clinics. (I, C)
patients from five countries with a high tuberculosis burden. AIDS
2006 20: 1275-1279.
Brust JC, Shah NS, Scott M, Chaiyachati K, Lygizos M, van der Multidrug-resistant TB service
Merwe TL, Bamber S, Radebe Z, Loveday M, Moll AP, Margot B, providing ART (but no
Lalloo UG, Friedland GH, Gandhi NR. Integrated, home-based comparator of referral to HIV
treatment for MDR-TB and HIV in rural South Africa: an alternate service for ART). (C)
model of care. Int J Tuberc Lung Dis 2012;16(8):998-1004.
Burgess AL, Fitzgerald DW, Severe P, Joseph P, Noel E, Rastogi N, Study describes cough screening
Johnson WD Jr, Pape JW. Integration of tuberculosis screening at an in a voluntary counselling and
HIV voluntary counselling and testing centre in Haiti. AIDS testing centre with referral for
2001;15(14):1875-9. TB evaluation. There is no
comparison to another model of
TB diagnostic service delivery.
(C)
Chan AK, Njala J, Kanyerere H, van Lettow M. Improved update of We included a more recent
ART following integration of TB and HIV services in a district in abstract (Chifundo 2010)
southern Malawi. 5th IAS Conference on HIV Pathogenesis and presenting more detailed data on
Treatment [Abstract no. CDD062] 2009. the same hospital. Kanyerere is
an author on both.
Coetzee D, Hilderbrand K, Goemaere E, Matthys F, Boelaert M. No comparison of ART in TB vs.
Integrating tuberculosis and HIV care in the primary care setting in HIV clinic to address PICO 4a.
South Africa. Trop Med Int Health 2004; 9: A11-15. No comparison of TB diagnosis
and/or treatment in HIV versus
TB clinics to address PICO 4b.
(I,C)
Desvarieux M, Hyppolite PR, Johnson WD, Pape JW. A novel No comparison of TB diagnosis
approach to directly observed therapy for tuberculosis in an HIV- and/or treatment in TB clinic.
endemic area. American Journal of Public Health 2001; 91: 138-141. (C)
Durovni B, Cavalcante SC, Saraceni V, Vellozo V, Israel G, King No description of diagnosis or
BS, Cohn S, Efron A, Pacheco AG, Moulton LH, Chaisson RE, treatment of active TB. (I)
16
Golub JE. The implementation of isoniazid preventive therapy in

HIV clinics: the experience from the TB/HIV in Rio (THRio) study.
AIDS 2010; 24(Suppl 5):S49-56.
Eibach D, et al. Decentralized integrated TB/HIV program in an No description of how the
unstable environment (Nimba county, Liberia). AIDS 2006 – XVI “integrated” care model worked;
International AIDS Conference [Abstract no. THPE0192]. no comparison is provided. (I, C)
Farmer P, Leandre F, Mukherjee J, Gupta R, Tarter L, Kim JY. Patient population had HIV
Community-based treatment of advanced HIV disease: introducing infection but not TB. (P)
DOT-HAART (directly observed therapy with highly active
antiretroviral therapy). Bull World Health Organ 2001; 79: 1145-
1151.
Friedland G, Churchyard GJ, Nardell E. Tuberculosis and HIV Review article
coinfection: current state of knowledge and research priorities. J
Infect Dis 2007;196(Suppl 1):S1-3.
Gandhi NR, Moll AP, Lalloo U, Pawinski R, Zeller K, Moodley P, No comparison is provided. (C)
Meyer E, Friedland G; Tugela Ferry Care and Research (TFCaRes)
Collaboration. Successful integration of tuberculosis and HIV
treatment in rural South Africa: the Sizonq’oba study. J Acquir
Immune Defic Syndr 2009;50(1):37-43.
Gasana M, Vandebriel G, Kabanda G, Tsiouris SJ, Justman J, Compares before/after for
Sahabo R, Kamugundu D, El-Sadr WM. Integrating tuberculosis and provider initiated HIV testing,
HIV care in rural Rwanda. Int J Tuberc Lung Dis 2008;12(3 Suppl but not ART. (I)
1):39-43.
Harris JB, Hatwiinda SM, Randels KM, Chi BH, Kancheya NG, Compared separate HIV and TB
Jham MA, Samungole KV, Tambatamba BC, Cantrell RA, Levy clinics before and after referral
JW, Kimerling ME, Reid SE. Early lessons from the integration of mechanisms were strengthened.
tuberculosis and HIV services in primary care centres in Lusaka, There is no comparison across
Zambia. Int J Tuberc Lung Dis 2008;12(7):773-9. delivery models. (I, C)
Hilderbrand K, et al. From TB/HIV services coordination to TB/HIV We included a more recent
service integration: different model of service delivery experimented (Brown, 2011) abstract by 5 of
in Khayelitsha, South Africa. 5th IAS Conference on HIV these authors from Khayelitsha
Pathogenesis and Treatment [Abstract no. TUPED118] 2009.
Jack C, Lalloo U, Karim QA, Karim SA, El-Sadr W, Cassol S, No comparison of referral to
Friedland G. A pilot study of once-daily antiretroviral therapy HIV clinics for ART. (C)
integrated with tuberculosis directly observed therapy in a resource-
limited setting. Journal of Acquired Immune Deficiency Syndromes
2004; 36: 929-934.
Kwange SO, Budambula NL. Effectiveness of anti-tuberculosis There is no comparison of TB
treatment among patients receiving highly active antiretroviral clinics providing ART versus
therapy at Vihiga district hospital in 2007. Indian J Med Microbiol. referring to specialized HIV
2010;28(1):21-5. clinics for ART to address PICO
4a. (I, C)
Médecins Sans Frontières. Khayelitsha annual activity report 2008– We included a more recent
2009: providing HIV/TB care at the primary health care level. abstract (Brown 2011) that
February 2010. provides more details on service
delivery model and patient
outcomes.
Miti S, Mfungwe V, Reijer P, Maher D. Integration of tuberculosis Did not specify HIV status of the
treatment in a community-based home care programme for persons patients; provides only an
living with HIV/AIDS in Ndola, Zambia. Int J Tuberc Lung Dis estimate of 70–80%. (P)
17
2003;7(9 Suppl 1):S92-8.

Njozing NB, Miguel SS, Tih PM, Hurtig AK. Assessing the No description or comparison of
accessibility of HIV care packages among tuberculosis patients in different models for providing
the Northwest Region, Cameroon. BMC Public Health 2010;10:129. ART. (I, C)
Odhiambo J, Kizito W, Njoroge A, Wambua N, Nganga L, Mburu This study does not address
M, Mansoer J, Marum L, Phillips E, Chakaya J, De Cock KM. PICO 4a because there is no
Provider-initiated HIV testing and counselling for TB patients and comparison of TB clinics
suspects in Nairobi, Kenya. Int J Tuberc Lung Dis 2008;12(3 Suppl providing ART versus referral to
1):63-8. HIV service. It does not speak to
PICO 4b because there is no
comparison of HIV services
diagnosing or treatment TB
versus referral to TB clinics. (I,
C)
Okot-Chono R, Mugisha F, Adatu F, Madraa E, Dlodlo R, Fujiwara Provides no data comparing
P. Health system barriers affecting the implementation of service delivery models. (I,C)
collaborative TB-HIV services in Uganda. Int J Tuberc Lung Dis
2009;13(8):955-61.
Roger I, et al. Integration of family planning, HIV and TB treatment Provides no comparison to TB
at primary health care centres in Kinshasa, Democratic Republic of nurses providing ART. (C) Note
the Congo. AIDS 2008 – XVII International AIDS Conference that we included an abstract (van
[Abstract no. WEPE0805]. Rie) by four of the same authors
presented the same year (2008)
at the UNION conference.
Sackoff JE, Torian LV, Frieden TR. TB prevention in HIV clinics in No comparison. (C)
New York City. Int J Tuberc Lung Dis 2001; 5: 123-128
Sweeney S, Obure CD, Maier CB, Greener R, Dehne K, Vassall A. Review of literature.
Costs and efficiency of integrating HIV/AIDS services with other
health services: a systematic review of evidence and experience.
Sexually Transmitted Infections 2012; 88: 85-99.
van Engelgem I, Telfer B, Kizito W, Ombeka VO, Raganoud M, Integration model not described.
Zachariah R. High acceptability of cotrimoxazole and antiretroviral No comparison is reported. (I, C)
treatment among HIV infected tuberculosis patients offered
integrated services in three health centres in Kibera, Nairobi.
Médecins Sans Frontières, 2008.
van Lettow M, Chan AK, Ginsburg AS, Tweya H, Gareta D, Njala J, No comparison of alternative
Kanyerere H, Phiri S, Idana I. Timing and uptake of ART during models of care. (C)
treatment for active tuberculosis in HIV co-infected adults in
Malawi. Public Health Action 2011; 1(1): 6-9.
Vassall A, Seme A, Compernolle P, Meheus F. Patient costs of No description of model of HIV
accessing collaborative tuberculosis and human immunodeficiency and TB services is provided, nor
virus interventions in Ethiopia. Int J Tuberc Lung Dis comparison of outcomes by how
2010;14(5):604-10. care is organized. (I, C)
Wannasorn P. Integrated TB and HIV services: an approach for There is no description or
quality improvement of care: AIDS 2006 – XVI International AIDS comparison of models for ART
Conference [Abstract no. THPE0201]. provision, so doesn’t address
Note that there was no abstract with this number in the 4th IAS PICO 4a. A multidisciplinary
conference; we found the same author and abstract number in IAC team began to provide
2006 (with a different title and additional authors). comprehensive HIV care
including “intensive TB
18
screening for HIV-infected

patients,” but there is no report
of where TB diagnosis is
confirmed now or before the
multidisciplinary team was
instituted, so this does not
address PICO 4b. (I, C)
Wiktor SZ, Sassan-Morokro M, Grant AD, Abouya L, Karon JM, Both arms received unsupervised
Maurice C, Djomand G, Ackah A, Domoua K, Kadio A, Yapi A, TB treatment from TB clinics
Combe P, Tossou O, Roels TH, Lackritz EM, Coulibaly D, De Cock (no comparison to HIV clinic—
KM, Coulibaly IM, Greenberg AE. Efficacy of trimethoprim- therefore does not address PICO
sulphamethoxazole prophylaxis to decrease morbidity and mortality 4b).
in HIV-1-infected patients with tuberculosis in Abidjan, Côte Neither arm received ART
d’Ivoire: a randomised controlled trial. Lancet (therefore does not address PICO
1999;353(9163):1469-75. 4a). (I, C)
World Health Organization. Report of a “lessons learnt” workshop No ART provided (so does not
on the six ProTEST pilot projects in Malawi, South Africa and address PICO 4a). No
Zambia. 2004. information on TB diagnosis in
HIV clinic versus TB clinic (so
does not address 4b). (I, C)
Zachariah R, Harries AD, Manzi M, Gomani P, Teck R, Phillips M, No comparison of TB clinic
Firmenich P. Acceptance of anti-retroviral therapy among patients providing ART versus referral to
infected with HIV and tuberculosis in rural Malawi is low and HIV clinic. (I, C)
associated with cost of transport. PLoS One 2006;1:e121.
Zwarenstein M, Fairall LR, Lombard C, Mayers P, Bheekie A, No comparison of TB diagnosis
English RG, Lewin S, Bachmann MO, Bateman E. Outreach and/or treatment at HIV clinics
education for integration of HIV/AIDS care, antiretroviral treatment, versus referral to TB clinics. (I,
and tuberculosis care in primary care clinics in South Africa: C)
PALSA PLUS pragmatic cluster randomised trial. BMJ 2011;
342:d2022
19

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82 © World Health Organization 2013

Title: Integration of HIV and TB services:

a Provision of HIV treatment and care at TB clinics

b Provision of TB treatment and care at HIV clinics

3. Flow diagram of screening process

Records after duplicates

Additional records Full-text articles assessed Full-text articles excluded

4.1. Observational studies

Outcome: ART uptake. See Fig. 7.

Outcome: timeliness of ART initiation. See Fig. 7.

Provides ART Refers for ART

Fig 2. After versus before

Kambale,* Pevzner, Howard, van

Refers for ART

Same nurse provides

Fig 3. After versus before

TB staff provides ART Refers for ART

Chifundo, Huerga, Morse, Mugo, Phiri

HIV-infected patients in care at HIV HIV-infected TB patients referred from TB

Treat and/or diagnose TB Refer for TB treatment and/or diagnosis

Fig 7. After creation of TB / HIV unit versus before

Refers for TB treatment

7. Bibliography of included studies

9. Pevzner E, Vandebriel G, Lowrance D, Gasana M, Finaly A. Evaluation of the rapid scale-up of

1. Bygrave H, Trivino L, Makakole L. TB/HIV integration: lessons learned from implementation of a

8. Excluded studies with reasons

Reference Reason for exclusion

(missing element population,

Golub JE. The implementation of isoniazid preventive therapy in

2003;7(9 Suppl 1):S92-8.

screening for HIV-infected

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