Prevalence of TB/HIV Co-Infection in Countries Except

China: A Systematic Review and Meta-Analysis

Junling Gao, Pinpin Zheng, Hua Fu*
School of Public Health, Fudan University, Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, China

Abstract
Background: TB and HIV co-epidemic is a major public health problem in many parts of the world. But the prevalence of TB/
HIV co-infection was diversified among countries. Exploring the reasons of the diversity of TB/HIV co-infection is important
for public policy, planning and development of collaborative TB/HIV activities. We aimed to summarize the prevalence of TB
and HIV co-infection worldwide, using meta-analysis based on systematic review of published articles.

Methods: We searched PubMed, Embase, and Web of Science for studies of the prevalence of TB/HIV co-infection. We also
searched bibliographic indices, scanned reference lists, and corresponded with authors. We summarized the estimates using
meta-analysis and explored potential sources of heterogeneity in the estimates by metaregression analysis.

Results: We identified 47 eligible studies with a total population of 272,466. Estimates of TB/HIV co-infection prevalence
ranged from 2.93% to 72.34%; the random effects pooled prevalence of TB/HIV co-infection was 23.51% (95% CI 20.91–
26.11). We noted substantial heterogeneity (Cochran’s x2 = 10945.31, p,0.0001; I2 = 99.58%, 95% CI 99.55–99.61).
Prevalence of TB/HIV co-infection was 31.25%(95%CI 19.30–43.17) in African countries, 17.21%(95%CI 9.97–24.46) in Asian
countries, 20.11%(95%CI 13.82–26.39) in European countries, 25.06%(95%CI 19.28–30.84) in Latin America countries and
14.84%(95%CI 10.44–19.24) in the USA. Prevalence of TB/HIV co-infection was higher in studies in which TB diagnosed by
chest radiography and HIV diagnosis based on blood analyses than in those which used other diagnostic methods, and in
countries with higher prevalence HIV in the general population than in countries with lower general prevalence.

Conclusions: Our analyses suggest that it is necessary to attach importance to HIV/TB co-infection, especially screening of
TB/HIV co-infection using methods with high sensitivity, specificity and predictive values in the countries with high HIV/
AIDS prevalence in the general population.

Citation: Gao J, Zheng P, Fu H (2013) Prevalence of TB/HIV Co-Infection in Countries Except China: A Systematic Review and Meta-Analysis. PLoS ONE 8(5):
e64915. doi:10.1371/journal.pone.0064915
Editor: Jialin Charles Zheng, University of Nebraska Medical Center, United States of America
Received January 20, 2013; Accepted April 21, 2013; Published May 31, 2013
Copyright: ß 2013 Gao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The study was sponsored by the Fundamental Research Funds for the Central Universities (grant number JJF201002). The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]

Introduction among HIV/AIDS population was 7.2% (4.2%–12.3%) [4]. So an

updated synthesis of the prevalence data from all other countries
The human immunodeficiency virus (HIV) pandemic presents a over the world would be important for public policy and planning
significant challenge to global tuberculosis (TB) control [1]. In and development of clinical services addressing the needs of TB
2011, 1.1 million (13%) of the 8.7 million people who developed and HIV/AIDS patients. It is also crucial to inform future projects
TB worldwide were HIV-positive [2]. TB is a leading killer among by identifying by identifying the reasons leading to the disparity of
people living with HIV. At least one in four deaths among people TB/HIV co-infection.
living with HIV can be attributed to TB [3]. To mitigate the dual We did a systematic review and meta-analysis to establish the
burden of TB/HIV in populations at risk of or affected by both prevalence of TB/HIV co-infection. We explored by meta
diseases, the World Health Organization (WHO) published a regression the reasons for variations between the primary studies
document on priority research questions in 2010 [3], and an and examined whether prevalence varied by year of publication,
updated policy on collaborative TB/HIV activities in 2012 [1], sex, study type, surveillance method, study size, study region, HIV
which emphasize the importance of surveillance of HIV among prevalence and TB prevalence of general population.
TB patients and surveillance of active TB patients among people
living with HIV in all countries. Methods
A wide range of estimates for the prevalence of TB/HIV co-
infection has been reported. However, to our knowledge, there Search Strategy and Selection Criteria
was only one study, which systematically evaluated the Chinese We searched PubMed, Embase and Web of Science with the
prevalence data of TB/HIV co-infection, indicated 0.9% (0.6%– term ‘‘co-infection and (tuberculosis or TB) and (HIV or AIDS or
1.4%) of TB patients were HIV infected, and the prevalence of TB human immunodeficiency virus or acquired immunodeficiency

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

syndrome)’’ to identify English articles on studies of the prevalence infection among TB patients), place (by comparing population-
of TB/HIV co-infection until Dec 31, 2011. We also searched based studies with hospital-based studies), study type (by compar-
relevant reference lists and relevant journals by hand and ing cross-sectional studies with cohort studies), study size (as a
corresponded with authors. Our analyses accorded with the continuous variable),and estimates of HIV and TB prevalence in
preferred reporting items for systematic reviews and meta-analyses the general population of the study country (as a continuous
(PRISMA) guidelines (when appropriate) for a systematic review of variable). Information about the prevalence of TB and HIV
prevalence [5]. infection in the general population was obtained from the UN
Cross-sectional or cohort studies addressing the prevalence of Millennium Development Goals Database [12,13]. We chose the
HIV infection among TB patients or the prevalence of TB among national data that most closely matched the year of publication of
HIV/AIDS population were included. If the study was reported in the study. We entered only factors that we deemed significant
duplicate, the article published earlier was included. Investigations individually (p,0.05) into a multiple regression model to avoid
were included irrespective of diagnostic methods, but mostly model instability. We did all analyses in Stata (version 12.1) with
included chest radiography for tuberculosis and blood tests for the commands metan (for random-effects meta-analysis specifying
HIV. Diagnoses based on questionnaires (e.g. self-report of disease three variables: double-arcsine-transformed prevalence, Wilson
status) were also included. CIs, and prevalence ratios) and metareg (for meta regression).
Review articles, and studies in languages other than English or
studies conducted in China, with ,50 participants, focusing on Results
incidence rates, and addressing specific high risk populations (e.g.
injecting drug users or offenders), were excluded. Our searches returned a total of 8489 records. After removal of
Two reviewers (JLG and PPZ) independently extracted duplicates and initial screening, we reviewed 138 papers in full.
information about geographical location, year of publication, After exclusion of ineligible reports, our final sample was 47 studies
method of sample selection, sample size, mean age range, (n = 272,466) were included in this review [11,14–59] (Figure 1).
surveillance method, diagnostic method, and numbers diagnosed The characteristics of the included studies were shown in Table
with tuberculosis or HIV from every eligible study. Disagreement S1.
was resolved by consensus between the two reviewers or through Six reports each were from the USA (226,904)[11,17–19,22,54]
consultation with the corresponding author, when necessary. If and Brazil (4,841) [29,37,42,46,49,56], five were from Nigeria
needed, we sought further clarifications from the authors of (2,520) [21,32,47,52,55], four each were from Ethiopia (2,609)
relevant studies. [28,34,36,44] and Spain (10,809) [14,24,26,40], three were from
India (1,825) [27,45,59], two each were from Iran (721) [43,53],
Statistical Analysis South Africa (374) [23,50], Zambia (2,309) [16,35], and
We calculated prevalence estimates with the variance stabilizing Zimbabwe (2,049) [15,58], and one each was from Cambodia
double arcsine transformation [6]. Because the inverse variance (441) [25], Trinidad and Tobago (121) [41], Israel (1,059) [51],
weight in fixed-effects meta-analyses is suboptimum when dealing Netherland (13,269) [30], Singapore (184) [48], Tanzania (233)
with binary data with low prevalence. Additionally, the trans- [39], Thailand(54) [31], Togo(569) [57], UK(157) [20], Uk-
formed prevalence is weighted very slightly towards 50%, and raine(968) [33], and Vietnam(450) [38]. Twenty-nine reports
studies with prevalence of zero can thus be included in the screened HIV infection among TB patients (n = 22,884)[15–
analysis. We used the Wilson method [7] to calculate 95% CIs 17,19–23,26–28,31,33–36,38,41,42,48,50–52,54–59], and eleven
around these estimates because the asymptotic method produces reports screened TB patients among HIV/AIDS patients
intervals which can extend below zero [8]. We estimated (12,627)[14,25,32,39,40,43–47,53], and the screening method
heterogeneity between studies with Cochran’s Q (reported as x2 was unknown in the remaining seven (236,955)
and p values) and the I2 statistic, which describes the percentage of [11,18,24,29,30,37,49]. Tuberculosis was diagnosed by combina-
variation between studies that is due to heterogeneity rather than tion of chest radiography and sputum culture in 9 studies
chance [9,10]. Unlike Q, I2 does not inherently depend on the (n = 6,562) [15,28,31,34,36,39,42,50,58], by combination of chest
number of studies included; values of 25%, 50%, and 75% show radiography, sputum culture and PPD skin test in 1 studies (459)
low, moderate, and high degrees of heterogeneity, respectively. [43], by sputum culture in 17 studies (14,769)[14,16,17,22,25–
Because heterogeneity was high (I2.75%), we used random-effects 27,32,33,38,41,44,45,47,48,52,54], by PPD skin test in 1 study
models for summary statistics [10]. These models (in which the (262) [53], by chest radiography in 1 study (2072) [35], by
individual study weight is the sum of the weight used in a fixed- combination of chest radiography and PPD skin test in 1 studies
effects model and between-study variability) produce study weights (161) [23]; the method of diagnosis was unknown in the remaining
that mainly show between-study variation and thus provide close seventeen(248,181)[11,18–21,24,29,30,37,40,46,49,51,55–57,59].
to equal weighting. We did a sensitivity analyses by excluding one HIV/AIDS was diagnosed by blood in 25 studies (14,953)[15–
largest study [11]. 17,20,21,23,27,28,33–36,39,41,43,44,47,48,51,52,55–59], the
method of diagnosis was unknown in the remaining twenty-two
Heterogeneity studies (256,913) [11,14,18,19,22,24–26,29–
We further investigated potential sources of heterogeneity by 32,37,38,40,42,45,46,49,50,53,54].
arranging groups of studies according to potentially relevant For study types, four were prospective cohort studies (n = 9,561)
characteristics and by meta regression analysis, which attempts to [20,28,40,58], nine studies were retrospective cohort studies
relate differences in effect sizes to study characteristics. Factors (242,934)[11,18,22,30,42,49–51,54], and the remaining thirty four
examined both individually and in multiple-variable models were studies were cross sectional studies (19,971)[14–17,19,21,23–
year of publication, sex (by comparing male samples with female 27,29,31–39,41,43–48,52,53,55–57,59], fifteen studies were pop-
samples), diagnosis method (by comparing studies that diagnosed ulation-based (255,093)[11,18,24,26,29,30,36–40,42,49,54,58],
TB by chest radiography and HIV by blood with others studies), and the other 32 studies were hospital-based (17,373)[14–17,19–
screening method (by comparing studies that screening TB 23,25,27,28,31–35,41,43–48,50–53,55–57,59], twenty one report-
patients among HIV/AIDS population with screening HIV ed data for men and women respectively (men = 13,004 wom-

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

Figure 1. Study flow.

doi:10.1371/journal.pone.0064915.g001

en = 23,811) [15,17,18,20,28,30,33,36,38,39,44,46–48,52–55,57– prevalence did not change. Whereas the random-effects pooled
59]. TB/HIV co-infection prevalence raised to 23.89% (95% CI
Estimates of TB/HIV co-infection prevalence ranged from 20.21–27.56) with substantial heterogeneity (x2 = 10401.68,
2.93% to 72.34% (Figure 2); heterogeneity was substantial p,0.0001; I2 = 99.57%, 95% CI 99.53–99.60).
(x2 = 10945.31, p,0.0001; I2 = 99.58%, 95% CI 99.55–99.61). Meta regression analyses were used in order to explore source of
The random effects pooled prevalence of TB/HIV co-infection heterogeneity. In individual variable meta regression analysis, the
was 23.51% (95% CI 20.91–26.11). The random effects pooled prevalence of TB/HIV co-infection was higher in studies in which
TB/HIV co-infection prevalence among TB patients was chest radiography was used for TB diagnosis and HIV diagnosis
25.23%(95%CI 18.58–31.89) with substantial heterogeneity based on blood analyses (coefficient = 13.70, p = 0.001) than in
(x2 = 5478.67, p,0.0001; I2 = 99.49%, 95% CI 99.43–99.54). those in which other diagnostic methods were used; general
And the random effects pooled TB/HIV co-infection prevalence population prevalence of TB (coefficient = 0.03, p = 0.001) and
among HIV/AIDS patients was 23.30%(95%CI 16.69–29.91) HIV (coefficient = 1.76, p,0.001) were positively related to the
with substantial heterogeneity (x2 = 850.64, p,0.0001; prevalence of TB/HIV co-infection, but high general population
I2 = 98.82%, 95% CI 98.51–99.07). Prevalence of TB/HIV co- prevalence of TB was not related to the prevalence of TB/HIV co-
infection was 31.25%(95%CI 19.30–43.17) in African countries, infection after multivariate meta regression(Table 1).
17.21%(95%CI 9.97–24.46) in Asian countries, 20.11%(95%CI
13.82–26.39) in European countries, 25.06%(95%CI 19.28–30.84) Discussion
in Latin America countries and 14.84%(95%CI 10.44–19.24) in
the USA (Figure 3). Our systematic review and meta-analysis of TB/HIV co-
As part of our sensitivity analyses, we excluded one large infection identified 47 studies of 272,466 individuals except China.
tuberculosis study [11]; estimates of TB/HIV co-infection Our main findings were that, a high prevalence of TB/HIV co-

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

Figure 2. Estimated prevalence of TB HIV co-infection by Screen methods.

doi:10.1371/journal.pone.0064915.g002

infection; TB/HIV co-infection prevalence was higher among TB patients and HIV/AIDS patients, especially in countries with high
patients than among HIV/AIDS patients, but which were not HIV prevalence or TB prevalence.
significantly different. Additionally, high general population Tuberculosis and HIV/AIDS can be worsened by each other.
prevalence of HIV/AIDS was related to higher prevalence of Tuberculosis is the most common opportunistic disease and cause
TB/HIV co-infection. These findings suggest that it should be of the death for those infected with HIV [60]. Similarly, HIV
paid more attention to screening TB/HIV co-infection among TB infection is one of the most important risk factors associated with
an increased risk of latent TB infection progressing to active TB

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

Figure 3. Estimated prevalence of TB and HIV co-infection by Region.

doi:10.1371/journal.pone.0064915.g003

disease [61,62]. So the WHO’s Policy on collaborative TB/HIV prevalence of TB/HIV co-infection in our meta-analysis is
activities recommends a combination of measures to reduce the 23.51% (95% CI 20.91–26.11), which is higher than the rate
burden of TB among HIV-infected individuals [1]. These (13%) reported by WHO in 2011 [2]. The reasons may be that,
measures include intensified case finding, isoniazid preventive more than half studies (26 of 47 studies) were conducted in African
therapy, and infection control and antiretroviral therapy. The and Asian countries (Ethiopia, Nigeria, South Africa, Zambia,

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

Table 1. Univariate and multivariate metaregression for prevalence of TB.

Metaregression coefficient (%)95%CI P

Univariate metaregression
Year of publication 20.27 20.88–0.34 0.381
Sex (male vs. female) 1.35 28.10–10.80 0.774
Diagnosis (TB by chest radiography and HIV by blood vs. other) 13.70 5.89–21.52 0.001
Screen (HIV from TB vs. TB from HIV) 24.34 212.65–3.97 0.302
Place (population-based vs. hospital-based) 25.24 212.45–1.97 0.152
Study type (cross-sectional vs. cohort) 1.43 23.61–6.46 0.575
Sample size ($500 vs. ,500) 20.21 27.09–6.67 0.952
Population prevalence of TB 0.03 0.01–0.05 0.001
Population prevalence of HIV/AIDS 1.76 1.14–2.37 ,0.001
Multivariate metaregression
Diagnosis (TB by chest radiography and HIV by blood vs. other) 3.32 2.46–12.10 0.035
Population prevalence of TB (per 100 000) 20.001 20.03–0.02 0.923
Population prevalence of HIV/AIDS (%) 1.62 0.71–2.53 0.001

doi:10.1371/journal.pone.0064915.t001

Zimbabwe, India and Thailand) with high general population associated with heterogeneity, such as history of TB and HIV/
prevalence of HIV and TB, while the HIV prevalence among AIDS, infectious routes of HIV or stages of AIDS, and future
people with TB is as high as 80% in some African countries [63]. research should describe samples in further detail.
However, this finding suggests case finding should be intensified Previous meta analysis of TB/HIV co-infection in China [4]
among TB patients and HIV/AIDS patients, because only 40% of reported a lower prevalence than that in our review, this may be
notified TB cases had a documented HIV test result in 2011 [2], because of low prevalence of HIV in China compared with that in
the percentage of people with TB who received an HIV test was countries where studies in our review were conducted. In addition,
just 26% in 2009 [63]. Gao and colleagues [4] reported lower summarized prevalence of
Our heterogeneity analyses generated several potentially HIV among TB patients for population-based studies. But our
important finding. Firstly, diagnostic method of chest radiography review didn’t find relationship between study place and prevalence
and blood was associated with significantly higher prevalence of of TB/HIV co-infection. An explanation could be demographic
TB/HIV co-infection than were other diagnostic methods. This factors of the study population, such as the gender and age
finding might be because of the higher sensitivity and specificity of distribution of subjects according to disease severity [66–68], but
chest radiography compared with sputum culture [64], which would need verification in future studies.
suggesting optimal TB algorithm to diagnose TB with high Because a meta-analysis has synthesized prevalence data of TB/
sensitivity, specificity and predictive values, that can be applied HIV co-infection in China [4],_ENREF_67 so we searched
across different settings and in patients with different TB and HIV prevalence data of TB/HIV co-infection in all other countries. But
disease burdens should be considered in the future. Secondly, only English articles were reviewed in our study, data published in
prevalence of TB/HIV co-infection was positively associated with other languages articles (e.g. French, Japanese) was unobtainable.
prevalence of HIV in the general population, which is consistent So collaboration of researchers from different language back-
with a previous study result that the rate of TB/HIV co-infection grounds is needed in the future. Second, due to the specific high-
depends on the prevalence of HIV infection in a community [36]. risk behaviors for TB and HIV infection, the selection of subjects
This result is potentially important from a public health might make results prone to potential selection bias even as we
perspective because it suggests it is should be paid more attention have excluded two studies performed among prisoners and
to screening TB/HIV co-infection among HIV/AIDS patients, injecting drug users. Another limitation of our systematic review
especially in countries with high HIV/AIDS prevalence of general is that, not all-necessary information, even age and HIV infection
population. This is also important from a preventive therapy routes stages of AIDS of the study population, could be obtained
because preventive TB therapy (any anti-TB drugs) reduces the from all included studies. Therefore, relevant stratified analyses
risk of active TB by 32% in people living with HIV [65], and could not be performed to disclose more detailed characteristics of
antiretroviral therapy reduces the individual risk of TB by 54% to the co-infection and its related risk factors.
92% and the population-based risk by 27% to 80% among people In conclusion, our analyses suggest that it is necessary to attach
living with HIV [1]. So HIV-infected patients should receive importance to HIV/TB co-infection, especially screening of TB/
antiretroviral therapy with optimal combination of antiretroviral HIV co-infection using methods with high sensitivity, specificity
and anti-TB therapy as early as possible. The substantial and predictive values in the countries with high HIV/AIDS
heterogeneity suggests that caution is necessary when pooled prevalence of general population. As prevalence of TB/HIV co-
estimates are used and emphasizes the need for careful description infection was positively associated with prevalence of HIV in the
of samples and diagnostic methods in surveys. Our sensitivity general population, and antiretroviral therapy is much helpful for
analyses showed that our overall results were not materially treatment of both diseases, so HIV-infected patients should receive
different when we excluded one study with largest sample size. antiretroviral therapy with as early as possible.
Other characteristics that we did not test might have been

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 Prevalence of TB/HIV Co-Infection: A Meta-Analysis

Supporting Information Author Contributions

Table S1 Studies of Prevalence of TB and HIV co- Conceived and designed the experiments: JLG PPZ HF. Performed the
experiments: JLG PPZ. Analyzed the data: JLG PPZ. Contributed
infection.
reagents/materials/analysis tools: JLG PPZ. Wrote the paper: JLG PPZ
(DOC) HF.

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