Email updates

Keep up to date with the latest news and content from BMC Infectious Diseases and BioMed Central.

Open Access Highly Accessed Research article

The proportions of people living with HIV in low and middle-income countries who test tuberculin skin test positive using either a 5 mm or a 10 mm cut-off: a systematic review

Andrew D Kerkhoff12*, Ankur Gupta3, Taraz Samandari4 and Stephen D Lawn23

Author Affiliations

1 School of Medicine and Health Sciences, The George Washington University, Washington, DC, USA

2 Desmond Tutu HIV Centre, Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa

3 Department of Clinical Research, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK

4 Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, Atlanta, Georgia, USA

For all author emails, please log on.

BMC Infectious Diseases 2013, 13:307  doi:10.1186/1471-2334-13-307

The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2334/13/307


Received:8 April 2013
Accepted:1 July 2013
Published:8 July 2013

© 2013 Kerkhoff et al.; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

A positive tuberculin skin test (TST) is often defined by skin induration of ≥10 mm in people who are HIV-seronegative. However, to increase sensitivity for detection of Mycobacterium tuberculosis infection in the context of impaired immune function, a revised cut-off of ≥5 mm is used for people living with HIV infection. The incremental proportion of patients who are included by this revised definition and the association between this proportion and CD4+ cell count are unknown.

Methods

The literature was systematically reviewed to determine the proportion of people living with HIV (PLWH) without evidence of active tuberculosis in low and middle-income countries who tested TST-positive using cut-offs of ≥5 mm and ≥10 mm of induration. The difference in the proportion testing TST-positive using the two cut-off sizes was calculated for all eligible studies and was stratified by geographical region and CD4+ cell count.

Results

A total of 32 studies identified meeting criteria were identified, providing data on 10,971 PLWH from sub-Saharan Africa, Asia and the Americas. The median proportion of PLWH testing TST-positive using a cut-off of ≥5 mm was 26.8% (IQR, 19.8-46.1%; range, 2.5-81.0%). Using a cut-off of ≥10 mm, the median proportion of PLWH testing TST-positive was 19.6% (IQR, 13.7-36.8%; range 0–52.1%). The median difference in the proportion of PLWH testing TST-positive using the two cut-offs was 6.0% (IQR, 3.4-10.1%; range, 0–37.6%). Among those with CD4+ cell counts of <200, 200–499 and ≥500 cells/μL, the proportion of positive tests defined by the ≥5 mm cut-off that were between 5.0 and 9.9 mm in diameter was similar (12.5%, 12.9% and 10.5%, respectively).

Conclusions

There is a small incremental yield in the proportion of PLWH who test TST-positive when using an induration cut-off size of ≥5 mm compared to ≥10 mm. This proportion was similar across the range of CD4+ cell strata, supporting the current standardization of this cut-off at all levels of immunodeficiency.

Keywords:
HIV; Tuberculin skin test; TST; Tuberculosis; CD4

Background

Tuberculin skin tests (TSTs) have for a long time been used to define likely Mycobacterium tuberculosis (MTB) infection, identify those who may benefit from isoniazid preventive therapy and aid diagnosis of tuberculosis (TB) disease, especially in children. While interferon gamma release assays (IGRAs) were developed to improve the diagnostic accuracy for MTB infection, the World Health Organization (WHO) does not recommend routine use of IGRAs in resource limited settings due to cost, technical complexity and limited utility [1].

The sensitivity of TSTs for detecting MTB infection is impaired among people living with HIV (PLWH) due to an attenuation of cell-mediated responses, including a reduction in memory CD4+ T cells at the TST site [2]. While a cut-off of ≥10 mm of induration is often used to define a positive TST among those who are HIV sero-negative, a cut-off of ≥5 mm is instead recommended by the US Centers for Disease Control and Prevention among PLWH to increase the sensitivity [3]. This revised cut-off is based on unpublished data from New York City in the 1980’s among just 23 AIDS patients with known TB disease of whom two had a TST of 5–9 mm induration while 13 had an induration ≥10 mm [4]. However, the incremental proportion of individuals defined as TST-positive when using this revised cut-off and the variables such as CD4+ cell count that might be associated with this proportion are not known.

Cobelens and colleagues [5] investigated TST responses among a large number of PLWH who were diagnosed as having active smear-positive pulmonary tuberculosis (TB) in Tanzania. Although just 71.2% of patients tested TST-positive when using the recommended cut-off of ≥5 mm of induration, this did not differ substantially from the proportion defined as positive using a cut-off of ≥10 mm of induration (64.3%) with a difference of just 6.9%. Thus, the altered cut-off only marginally reduced the number of false-negative tests. The authors concluded from their data that loss of sensitivity of the TST in PLWH is predominantly attributable to anergy (ie an all-or-nothing phenomenon) rather than due to a gradual diminution in TST diameter during progressive immunodeficiency. However, this study was conducted solely among PLWH who had active TB and these findings cannot necessarily be extrapolated to those with latent MTB infection and any association with CD4+ cell count was not defined.

We previously conducted a systematic review of the literature to ascertain the proportions of PLWH who tested TST-positive using the conventional cut-off of ≥5 mm of induration [6]. In the present systematic review, we determined the proportions of PLWH testing TST-positive using cut-offs of ≥5 mm and ≥10 mm cut-off and the relationship with CD4+ cell count.

Methods

Search strategy

The search strategy has been described in detail elsewhere [6]. In brief, we searched Embase, Global Health, Medline and Web of Science for relevant citations using a combination of MeSH and free text search terms according to a predetermined search criteria. The search was restricted to articles from January 1, 1990 to February 5, 2012 as an initial search demonstrated no relevant citations prior to this period. The first search set was created using comprehensive search terms for tuberculin skin test, latent tuberculosis and isoniazid preventive therapy and were combined using “or.” A second set was created for HIV/AIDS using comprehensive search terms. These two sets were then combined using “and.” Next, this set was combined with a low and middle-income country (LMIC) set (using the World Bank list of economies as of 01 July 2011) [7] using “and.” All citations were then limited to articles published in English and among humans.

Studies eligible for inclusion were those that were conducted in LMIC’s, included only PLWH who were at least 15 years of age, presented data for patients without evidence of active TB disease, and presented the proportion of those testing TST-positive current using a induration cut-off size of both ≥5 mm and ≥10 mm. Studies were also required to have at least 30 participants meeting the above criteria to limit imprecision around the point estimates. Studies utilizing two-step TST testing were excluded. All studies meeting the aforementioned criteria were included regardless of patient ART status at enrolment.

Citations identified through the search process were compiled into Endnote where duplicate citations were removed. Titles and abstracts were screened for study inclusion. Potentially relevant full-text citations were entered into an Excel spreadsheet and the full-texts were obtained. Two readers (ADK and SDL) carefully reviewed all full-text publications for study inclusion. Additional studies met the inclusion criteria following provision of additional data by the authors as previously described [6].

Data extraction

Study characteristics from eligible studies were abstracted directly into a structured Microsoft Excel spreadsheet. Variables recorded included: title, authors, year of publication, study period, study location, clinical setting, mean or median patient age, bacille Calmette et Guerin (BCG) vaccine scar status, ART status, special or potentially non-generalizable populations and the total number of eligible PLWH who underwent TST testing (and returned to have their results read) and the total number PLWH testing TST-positive using both a ≥5 mm and a ≥10 mm induration size. When TST-results using both a ≥5 mm and a ≥10 mm cut-off stratified by CD4+ cell counts (<200, 200–499 and ≥500 cells/μL) were available, these were also recorded.

The quality of studies was independently assessed by two reviewers (ADK and SDL) using a graded checklist [6]. A study receiving 70% of available points was considered to be of “good quality”, 50-70% was considered “medium quality” and less than 50% was considered “lower quality.” We also assessed the risk of bias in individual studies as well as across all included studies.

Statistical analysis

All statistical analysis was completed using STATA version 10.0. The difference in the proportion of those testing TST-positive using a ≥5 mm versus a ≥10 mm cut-off was calculated for all eligible studies and chi-squared tests were used to compare these proportions. Differences in the proportions of PLWH testing TST-positive by each cut-off size were then plotted using a forest plot and were stratified by geographic region and CD4+ cell count. Pooled estimates of overall data or stratified data were not derived due to substantial heterogeneity between studies as indicated by large I2 values [8].

Results

Of the 3,095 potential citations identified in the literature search, 254 were selected for full-text review (Figure 1). After concluding a full-text review, 24 articles met the pre-defined inclusion criteria and an additional 8 articles met inclusion criteria due to unpublished data provided by authors for a previous study. In all, 32 publications provided data from 34 unique study populations and were published between 1992 and 2011 (Additional file 1). Among included publications, 14 study populations were from Africa, 8 from the Americas and 12 from Asia. The TB prevalence in counties in which the studies were conducted ranged from 0.19-785 cases per 100,000 population and the majority (62%; 21/34) of study populations were from high-prevalence TB countries (estimated TB prevalence >100 cases per 100,000 population).

thumbnailFigure 1. Overview of eligible studies containing data on the proportion of people living with HIV testing TST-positive using a ≥5 mm and ≥10 mm cut-off size.

Additional file 1. Characteristics of studies presenting data on the proportion of HIV-infected patients who tested TST-positive using a ≥5 mm and ≥10 mm cut-off size.

Format: DOC Size: 165KB Download file

This file can be viewed with: Microsoft Word ViewerOpen Data

The mean/median age among patients in eligible studies ranged from 22–42 years. The proportions of PLWH on ART at the time of TST assessment was reported for 18 study populations and an additional six study populations were assumed to be ART naïve as the studies were conducted prior to national ART implementation. Among these 24 populations, ART was received by a proportion of the participants in only 9 studies and this proportion varied from 1% to 100% (median 58%). Nine publications were of high quality, 12 studies of medium quality and 11 studies of low quality, as determined by a quality assessment checklist.

Difference in patients testing TST-positive using a ≥5 mm versus ≥10 mm cut-off size

Overall, there were 10,971 PLWH with TST results from 34 study populations; 4,880 were from sub-Saharan Africa, 2,247 from the Americas and 3,844 from Asia. All studies reported the proportion of individuals testing TST-positive using both a 5 mm and 10 mm cut-off (Table 1).

Table 1. The proportion of people living with HIV who tested TST-positive using a ≥5 mm and ≥10 mm cutoff size and the difference between these two proportions

The median proportion of PLWH testing TST-positive using a cut-off of ≥5 mm was 26.8% (IQR, 19.8-46.1%; range 2.5-81.0%). There was considerable heterogeneity with regard to regional differences in the proportion of patients testing TST-positive. The median proportions of patients testing TST-positive in sub-Saharan Africa, the Americas and Asia were 36.8% (IQR, 24.7-51.0%; range, 20.2-57.5%), 17.8% (IQR, 10.6-22.9%; range, 2.5-58.1%), and 27.3% (IQR, 20.3-45.8%; range, 3.2-81.0%), respectively.

When a cut-off of ≥10 mm was used, the median proportion of patients testing TST-positive was 19.6% (IQR, 13.7-36.8%; range, 0–52.1%). Strong regional differences in the proportion of patients TST-positive were again noted. Patients in sub-Saharan Africa had a median TST-positive proportion of 31.5% (IQR, 20.3-39.0%; range, 16.2-52.1%) compared to 12.4% (IQR, 5.2-18.6%; range, 0–46.5%) in the Americas and 15.4% (IQR, 13.3-36.3%; range, 3.2-47.4%) in Asia.

The median difference observed in the proportion of those testing TST-positive using a cut-off size of ≥5 mm versus ≥10 mm was 6.0% (IQR, 3.4-10.1%; range 0–37.6%). When stratified by geographic region, the median difference in the proportion of patients testing TST-positive using a 5 mm versus a 10 mm cut-off was 4.7% (IQR, 3.1-7.9%, range, 1.0-18.6%), 5.7% (IQR, 3.6-9.8%, range, 0.8-11.6%) and 7.3% (IQR, 4.4-17.0%, range, 0–37.6%) for Africa, the Americas and Asia respectively. The overall difference in the proportions of patients testing TST positive (Figure 2a) and stratified according to geographic region (Figure 2b) was demonstrated in forest plots.

thumbnailFigure 2. Forest plot showing the difference in proportions (%, 95% CI) of people living with HIV testing TST-positive using a ≥5 mm versus a ≥10 mm cut-off size in (a) all study populations (n = 34) and (b) with data grouped according to region.

Association with CD4+ cell counts

Nine studies with a total of 5,107 PLWH reported the proportion of those testing TST-positive using both a ≥5 mm and a ≥10 mm cut-off size stratified by CD4+ cell counts at <200, 200–499, ≥500 (Table 2). These CD4+ cell count stratified data are shown in a forest plot (Figure 3). The median difference in the proportion of PLWH testing TST-positive using the two induration cut-off sizes was 2.0% (range, 0–10.7%; IQR, 0–7.8%), 3.5% (range, 1.5-7.8%; IQR, 2.7-4.4%) and 6.0% (range, 2.6-20.9%; IQR, 4.9-9.6%) among those with CD4+ cell counts <200, 200–499, ≥500 cells/μL, respectively. The corresponding proportions of positive tests defined by the ≥5 mm cut-off that were between 5.0 and 9.9 mm in diameter were 12.5% (IQR, 0–16.0), 12.9% (IQR, 7.6-15.2), 10.5% (IQR, 9.1-28.5), respectively [9-40].

Table 2. The proportion of people living with HIV who tested TST-positive using a ≥5 mm and ≥10 mm cutoff size stratified by CD4+ cell count categories <200, ≥200, 200–499 and ≥500 cells/μL

Discussion

This study found that among 10,971 patients without active TB in 34 different study populations, the incremental yield of patients defined as TST-positive when using a ≥5 mm cut-off rather than a ≥10 mm cut-off was just 6.0%. This suggests that using the modified cut-off had only a modest effect on increasing the proportion of PLWH who tested TST-positive. Importantly, this proportion was similar across the range of CD4+ cell count strata and also across different geographic regions.

thumbnailFigure 3. Forest plot showing the difference in proportions (%, 95% CI) of people living with HIV testing TST-positive using a ≥5 mm versus a ≥10 mm cut-off size with data grouped according to CD4+ cell count strata (<200, 200–499 and ≥500 cells/μL).

Our findings of a 6% incremental proportion associated with the use of the revised TST cut-off among patients without active TB are very similar to those of Cobelens and colleagues [5] who reported a 7% increment among patients with active TB in Tanzania. This suggests that the small differences observed in the proportion of PLWH testing TST-positive using the two cut-off sizes are generalizable regardless of TB infection or disease status.

A recent systematic review and meta-analysis [41] investigated the utility of ≥5 mm and ≥10 mm TST cut-off sizes to predict the progression from latent infection to active TB disease. Among five studies in which the HIV status of patients was largely unknown, the unadjusted incidence rate ratio of tuberculosis in TST-positive patients was 1.43 (95% CI, 0.75-2.72) when a cut-off of ≥5 mm was used and 1.60 (95% CI, 0.94-2.72) when a cut-off ≥10 mm was applied. Thus, neither cut-off size better predicted the risk for progression to active TB disease. However, because the HIV status of the patients included in these studies was negative or largely unknown, it remains unclear whether these findings are generalizable to PLWH.

TSTs rather than IGRAs are the WHO-recommended assay for use in LMICs for detecting latent tuberculosis infection among PLWH prior to isoniazid preventive therapy [42]. Although use of TST is recommended, it remains unknown whether a ≥5 mm or ≥10 mm cut-off size better defines those who will benefit from IPT. A meta-analysis [43] among PLWH demonstrated that among those with a TST induration of ≥5 mm in diameter, IPT was associated with a TB risk reduction of 64% (95% CI, 39-78 %). However, all studies in this meta-analysis defined TST-positivity using a ≥5 mm cut-off size and thus it is not known whether those with a 5.0-9.9 mm induration gain benefit from IPT. An individual patient meta-analysis of data from randomized trials of isoniazid preventive therapy may be able to define this.

Strengths of this study include a comprehensive search strategy that utilized four different study databases. There were more than 10,000 patients from 34 unique study populations from many countries and geographic regions. Also, a number of variables potentially influencing differences in the proportion of TST-positive patients were recorded and summarized where possible. There were also several limitations. The reliability of TST assessment could not be assessed. Additionally, methods for excluding TB disease were not standardized among included studies. Heterogeneity in the data precluded the calculation of pooled summary estimates.

Conclusion

In conclusion, using a ≥5 mm cut-off among PLWH resulted in only a modest increase in the proportion testing TST-positive when compared to a cut-off size of ≥10 mm and this finding concurs with a similar study that was conducted among patients with active TB. The difference in the proportion of PLWH testing TST-positive when using the two different cut-off sizes was similar across the range of CD4+ cell count strata suggesting use of this cut-off across the spectrum of immunodeficiency.

Competing interest

The authors have no conflicts of interest to declare.

Authors’ contributions

ADK initiated the study. ADK designed the search strategy. ADK ran the searches and selected and graded the studies with SDL. ADK, AG and SDL did the data synthesis. ADK and SDL wrote the manuscript and all other co-authors contributed to and approved the final draft.

Acknowledgements

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the U.S. Centers for Disease Control and Prevention.

Funding

SDL is funded by the Wellcome Trust, London, UK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  1. World Health Organization: Use of tuberculosis interferon-gamma release assays (IGRAs) in low- and middle- income countries. Geneva, Switzerland: World Health Organization; 2011:1-70. OpenURL

  2. Sarrazin H, Wilkinson KA, Andersson J, Rangaka MX, Radler L, Van Veen K, Lange C, Wilkinson RJ: Association between tuberculin skin test reactivity, the memory CD4 cell subset, and circulating FoxP3-expressing cells in HIV-infected persons.

    J Infect Dis 2009, 199:702-710. PubMed Abstract | Publisher Full Text OpenURL

  3. Centers for Disease Control and Prevention: Targeted tuberculin testing and treatment of latent tuberculosis infection.

    MMWR 2000, 49(RR6):1-51. PubMed Abstract | Publisher Full Text OpenURL

  4. Centers for Disease Control (CDC): Tuberculosis and human immunodeficiency virus infection: recommendations of the Advisory Committee for the Elimination of Tuberculosis (ACET).

    MMWR 1989, 38:236–8-243–50. PubMed Abstract OpenURL

  5. Cobelens FG, Egwaga SM, Van Ginkel T, Muwinge H, Matee MI, Borgdorff MW: Tuberculin skin testing in patients with HIV infection: limited benefit of reduced cutoff values.

    Clin Infect Dis 2006, 43:634-639. PubMed Abstract | Publisher Full Text OpenURL

  6. Kerkhoff AD, Kranzer K, Samandari T, Nakiyingi-Miiro J, Whalen CC, Harries AD, Lawn SD: Systematic review of TST responses in people living with HIV in under-resourced settings: implications for isoniazid preventive therapy.

    PLoS One 2012, 7:e49928. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  7. World Bank Website

    2011.

    Available: http://data.worldbank.org/about/country-classifications/country-and-lending-groups webcite

  8. Higgins JPT, Thompson SG: Quantifying heterogeneity in a meta-analysis.

    Statist Med 2002, 21:1539-1558. Publisher Full Text OpenURL

  9. Allen S, Batungwanayo J, Kerlikowske K, Lifson AR, Wolf W, Granich R, Taelman H, Van De Perre P, Serufilira A, Bogaerts J: Two-year incidence of tuberculosis in cohorts of HIV-infected and uninfected urban Rwandan women.

    Am Rev Respir Dis 1992, 146:1439-1444. PubMed Abstract | Publisher Full Text OpenURL

  10. Aisu T, Raviglione MC, Van Praag E, Eriki P, Narain JP, Barugahare L, Tembo G, McFarland D, Engwau FA: Preventive chemotherapy for HIV-associated tuberculosis in Uganda: an operational assessment at a voluntary counselling and testing centre.

    AIDS 1995, 9:267-273. PubMed Abstract OpenURL

  11. Duncan LE, Elliott AM, Hayes RJ, Hira SK, Tembo G, Mumba GT, Ebrahim SH, Quigley M, Pobee JO, McAdam KP: Tuberculin sensitivity and HIV-1 status of patients attending a sexually transmitted diseases clinic in Lusaka, Zambia: a cross-sectional study.

    Trans R Soc Trop Med Hyg 1995, 89:37-40. PubMed Abstract | Publisher Full Text OpenURL

  12. Fordham Von Reyn C, Arbeit RD, Tosteson AN, Ristola MA, Barber TW, Waddell R, Sox CH, Brindle RJ, Gilks CF, Ranki A, Bartholomew C, Edwards J, Falkinham JO, O’Connor GT: The international epidemiology of disseminated Mycobacterium avium complex infection in AIDS. International MAC Study Group.

    AIDS 1996, 10:1025-1032. PubMed Abstract | Publisher Full Text OpenURL

  13. Diagbouga S, Fumoux F, Ledru E, Sanou PT, Barro D, Marchal G: Lack of direct correlation between CD4 T-lymphocyte counts and induration sizes of the tuberculin skin test in human immunodeficiency virus type 1 seropositive patients.

    Int J Tuberc Lung Dis 1998, 2:317-323. PubMed Abstract | Publisher Full Text OpenURL

  14. Waddell RD, Von CF R, Baboo KS, Mwinga A, Chintu C, Zumla A: The effects of BCG immunization and human immunodeficiency virus infection on dual skin test reactions to purified protein derivative and Mycobacterium avium sensitin among adults in Zambia.

    Int J Tuberc Lung Dis 1999, 3:255-260. PubMed Abstract | Publisher Full Text OpenURL

  15. Mtei L, Matee M, Herfort O, Bakari M, Horsburgh CR, Waddell R, Cole BF, Vuola JM, Tvaroha S, Kreiswirth B, Pallangyo K, Reyn Von CF: High rates of clinical and subclinical tuberculosis among HIV-infected ambulatory subjects in Tanzania.

    Clin Infect Dis 2005, 40:1500-1507. PubMed Abstract | Publisher Full Text OpenURL

  16. Tegbaru B, Wolday D, Messele T, Legesse M, Mekonnen Y, Miedema F, van Baarle D: Tuberculin skin test conversion and reactivity rates among adults with and without human immunodeficiency virus in urban settings in Ethiopia.

    Clin Vaccine Immunol 2006, 13:784-789. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  17. Rangaka MX, Diwakar L, Seldon R, Van Cutsem G, Meintjes GA, Morroni C, Mouton P, Shey MS, Maartens G, Wilkinson KA, Wilkinson RJ: Clinical, immunological, and epidemiological importance of antituberculosis T cell responses in HIV-infected Africans.

    Clin Infect Dis 2007, 44:1639-1646. PubMed Abstract | Publisher Full Text OpenURL

  18. Karam F, Mbow F, Fletcher H, Senghor CS, Coulibaly KD, Lefevre AM, Ngom Gueye NF, Dieye T, Sow PS, Mboup S, Lienhardt C: Sensitivity of IFN-γ release assay to detect latent tuberculosis infection is retained in HIV-infected patients but dependent on HIV/AIDS progression.

    PLoS One 2008, 3:e1441. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  19. Hanifa Y, Grant AD, Lewis J, Corbett EL, Fielding K, Churchyard G: Prevalence of latent tuberculosis infection among gold miners in South Africa.

    Int J Tuberc Lung Dis 2009, 13:39-46. PubMed Abstract | Publisher Full Text OpenURL

  20. Leidl L, Mayanja-Kizza H, Sotgiu G, Baseke J, Ernst M, Hirsch C, Goletti D, Toossi Z, Lange C: Relationship of immunodiagnostic assays for tuberculosis and numbers of circulating CD4+ T-cells in HIV infection.

    Eur Respir J 2010, 35:619-626. PubMed Abstract | Publisher Full Text OpenURL

  21. Oni T, Burke R, Tsekela R, Bangani N, Seldon R, Gideon HP, Wood K, Wilkinson KA, Ottenhoff THM, Wilkinson RJ: High prevalence of subclinical tuberculosis in HIV-1-infected persons without advanced immunodeficiency: implications for TB screening.

    Thorax 2011, 66:669-673. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  22. Samandari T, Agizew TB, Nyirenda S, Tedla Z, Sibanda T, Shang N, Mosimaneotsile B, Motsamai OI, Bozeman L, Davis MK, Talbot EA, Moeti TL, Moffat HJ, Kilmarx PH, Castro KG, Wells CD: 6-month versus 36-month isoniazid preventive treatment for tuberculosis in adults with HIV infection in Botswana: a randomised, double-blind, placebo-controlled trial.

    Lancet 2011, 377:1588-1598. PubMed Abstract | Publisher Full Text OpenURL

  23. Espinal MA, Reingold AL, Lavandera M: Effect of pregnancy on the risk of developing active tuberculosis.

    J Infect Dis 1996, 173:488-491. PubMed Abstract | Publisher Full Text OpenURL

  24. García-García ML, Valdespino-Gómez JL, García-Sancho C, Mayar-Maya ME, Palacios-Martínez M, Balandrano-Campos S, Escobar-Gutiérrez A, Peruga A, Weissenbacher M, Daniels E: Underestimation of Mycobacterium tuberculosis infection in HIV-infected subjects using reactivity to tuberculin and anergy panel.

    Int J Epidemiol 2000, 29:369-375. PubMed Abstract | Publisher Full Text OpenURL

  25. Miranda A, Morgan M, Jamal L, Laserson K, Barreira D, Silva G, Santos J, Wells C, Paine P, Garrett D: Impact of antiretroviral therapy on the incidence of tuberculosis: the Brazilian experience, 1995–2001.

    PLoS One 2007, 2:e826. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  26. Balcells ME, Pérez CM, Chanqueo L, Lasso M, Villanueva M, Espinoza M, Villarroel L, García P: A comparative study of two different methods for the detection of latent tuberculosis in HIV-positive individuals in Chile.

    Int J Infect Dis 2008, 12:645-652. PubMed Abstract | Publisher Full Text OpenURL

  27. Gutierrez E, Gomes V, Picone C, Suga H, Atomiya A: Active tuberculosis and Mycobacterium tuberculosislatent infection in patients with HIV/AIDS.

    HIV Med 2009, 10:564-572. PubMed Abstract | Publisher Full Text OpenURL

  28. Baboolal S, Ramoutar D, Akpaka PE: Comparison of the QuantiFERON®-TB Gold assay and tuberculin skin test to detect latent tuberculosis infection among target groups in Trinidad & Tobago.

    Rev Panam Salud Publica 2010, 28:36-42. PubMed Abstract OpenURL

  29. Moura LC, Ximenes RA, Ramos HL, Filho DBM, Freitas CD, Silva RM, Coimbra I, Batista JDL, Montarroyos UR, Militão DFP, Albuquerque M: An evaluation of factors associated with taking and responding positive to the tuberculin skin test in individuals with HIV/AIDS.

    BMC Publ Health 2011, 11:687. BioMed Central Full Text OpenURL

  30. Suwanagool S, Chuenarom V, Pechthanon L, Sonjai A, Leelarasamee A, Pathrakom C: A comparative study of tuberculin skin test reactivity between asymptomatic HIV-1 seropositive subjects and healthy volunteers.

    Asian Pac J Allergy Immunol 1995, 13:139-144. PubMed Abstract OpenURL

  31. Yanai H, Uthaivoravit W, Mastro TD, Limpakarnjanarat K, Sawanpanyalert P, Morrow RH, Nieburg P: Utility of tuberculin and anergy skin testing in predicting tuberculosis infection in human immunodeficiency virus-infected persons in Thailand.

    Int J Tuberc Lung Dis 1997, 1:427-434. PubMed Abstract | Publisher Full Text OpenURL

  32. Sawhney M, Sharma YK: Significance of tuberculin testing in HIV infection: An Indian perspective.

    Medical Journal Armed Forces India 2006, 62:104-107. Publisher Full Text OpenURL

  33. Gupta A, Nayak U, Ram M, Bhosale R, Patil S, Basavraj A, Kakrani A, Philip S, Desai D, Sastry J, Bollinger RC, Byramjee J: Medical College-Johns Hopkins University Study Group: Postpartum tuberculosis incidence and mortality among HIV-infected women and their infants in Pune, India, 2002–2005.

    Clin Infect Dis 2007, 45:241-249. PubMed Abstract | Publisher Full Text OpenURL

  34. Swaminathan S, Subbaraman R, Venkatesan P, Subramanyam S, Kumar SR, Mayer KH, Narayanan PR: Tuberculin skin test results in HIV-infected patients in India: implications for latent tuberculosis treatment.

    Int J Tuberc Lung Dis 2008, 12:168-173. PubMed Abstract | Publisher Full Text OpenURL

  35. Davarpanah M, Rasti M, Mehrabani D, Allahyari S, Neirami R, SaberiFiroozi M: Association between PPD and QuantiFERON gold TB test in TB infection and disease among HIV infected.

    Iran Red Crescent Med J 2009, 11:71-75. OpenURL

  36. Davarpanah M, Rafiee G, Mehrabani D: The prevalence of M. tuberculosis infection and disease in HIV positive individuals in Shiraz, Southern Iran.

    Iran Red Crescent Med J 2009, 11:199-202. OpenURL

  37. Jiang W, Shao L, Zhang Y, Zhang S, Meng C, Xu Y, Huang L, Wang Y, Wang Y, Weng X, Zhang W: High-sensitive and rapid detection of Mycobacterium tuberculosis infection by IFN-gamma release assay among HIV-infected individuals in BCG-vaccinated area.

    BMC Immunol 2009, 10:31. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  38. Zhang M, Wang H, Liao M, Chen X, Graner M, Zhu X, Zhang J, Yang Q, Lu H, Zhou B, Chen X: Diagnosis of latent tuberculosis infection in bacille Calmette-Guérin vaccinated subjects in China by interferon-gamma ELISpot assay.

    Int J Tuberc Lung Dis 2010, 14:1556-1563. PubMed Abstract | Publisher Full Text OpenURL

  39. Kabeer BSA, Sikhamani R, Raja A: Comparison of interferon gamma–inducible protein-10 and interferon gamma–based QuantiFERON TB Gold assays with tuberculin skin test in HIV-infected subjects.

    Diagn Microbiol Infect Dis 2011, 71:236-243. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  40. Nguyen DTM, Hung NQ, Giang LT, Dung NH, Lan NTN, Lan NN, Yen NTB, Bang ND, Ngoc DV, Trinh LTT, Beasley RP, Ford CE, Hwang L-Y, Graviss EA: Improving the diagnosis of pulmonary tuberculosis in HIV-infected individuals in Ho Chi Minh City, Viet Nam.

    Int J Tuberc Lung Dis 2011, 15:1528-1534. PubMed Abstract | Publisher Full Text OpenURL

  41. Rangaka MX, Wilkinson KA, Glynn JR, Ling D, Menzies D, Mwansa-Kambafwile J, Fielding K, Wilkinson RJ, Pai M: Predictive value of interferon-γ release assays for incident active tuberculosis: a systematic review and meta-analysis.

    Lancet Infect Dis 2012, 12:45-55. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  42. World Health Organization:

    Guidelines for intensified tuberculosis case-finding and isoniazid preventative therapy for people living with HIV in resource-contrained settings. 2011, 1-187. OpenURL

  43. Akolo C, Adetifa I, Shepperd S, Volmink J: Treatment of latent tuberculosis infection in HIV infected persons.

    Cochrane Database Syst Rev 2010, CD000171. OpenURL

Pre-publication history

The pre-publication history for this paper can be accessed here:

http://www.biomedcentral.com/1471-2334/13/307/prepub