Comparison of Interferon-γ Release Assays and the Tuberculin Skin Test for Diagnosis of Tuberculosis in Human Immunodeficiency Virus: A Systematic Review
Rick Varma (Prince of Wales Hospital)
Jeffrey J. Post (Prince of Wales Hospital)
- Downloaded
- Viewed
Abstract
Background: It remains uncertain if interferon-γ release assays (IGRAs) are superior to the tuberculin skin test (TST) for the diagnosis of active tuberculosis (TB) or latent tuberculosis infection (LTBI) in immunosuppressed populations including people with human immunodeficiency virus (HIV) infection. The purpose of this study was to systematically review the performance of IGRAs and the TST in people with HIV with active TB or LTBI in low and high prevalence TB countries. Methods: We searched the MEDLINE database from 1966 through to January 2017 for studies that compared results of the TST with either the commercial QuantiFERON-TB Gold in Tube (QFTGT) assay or previous assay versions, the T-SPOT.TB assay or in-house IGRAs. Data were summarized by TB prevalence. Tests for concordance and differences in proportions were undertaken as appropriate. The variation in study methodology was appraised. Results: Thirty-two studies including 4,856 HIV subjects met the search criteria. Fourteen studies compared the tests in subjects with LTBI in low TB prevalence settings. The QFTGT had a similar rate of reactivity to the TST, although the first-generation version of that assay was reactive more commonly. IGRAs were more frequently positive than the TST in HIV infected subjects with active TB. There was considerable study methodology and population heterogeneity, and generally low concordance between tests. Both the TST and IGRAs were affected by CD4 T-cell immunodeficiency. Conclusion: Our review of comparative data does not provide robust evidence to support the assertion that the IGRAs are superior to the TST when used in HIV infected subjects to diagnose either active TB or LTBI.
- keywords
- Interferon-Gamma Release Assays, Tuberculin Test, HIV Infection, Latent Tuberculosis, Review, Systematic
Reference
World Health Organization. Global tuberculosis control: WHO report 2011. Geneva: World Health Organization; 2011.
Targeted tuberculin testing and treatment of latent tuberculosis infection. This official statement of the American Thoracic Society was adopted by the ATS Board of Directors, July 1999. This is a Joint Statement of the American Thoracic Society (ATS) and the Centers for Disease Control and Prevention (CDC). This statement was endorsed by the Council of the Infectious Diseases Society of America. (IDSA), September 1999, and the sections of this statement. Am J Respir Crit Care Med 2000;161(4 Pt 2):S221-47.
Wang L, Turner MO, Elwood RK, Schulzer M, FitzGerald JM. A meta-analysis of the effect of Bacille Calmette Guerin vaccination on tuberculin skin test measurements. Thorax 2002;57:804-9.
Telisinghe L, Amofa-Sekyi M, Maluzi K, Kaluba-Milimo D, Cheeba-Lengwe M, Chiwele K, et al. The sensitivity of the QuantiFERON(R)-TB Gold Plus assay in Zambian adults with active tuberculosis. Int J Tuberc Lung Dis 2017;21:690-6.
Richeldi L. An update on the diagnosis of tuberculosis infection. Am J Respir Crit Care Med 2006;174:736-42.
Brock I, Ruhwald M, Lundgren B, Westh H, Mathiesen LR, Ravn P. Latent tuberculosis in HIV positive, diagnosed by the M. tuberculosis specific interferon-gamma test. Respir Res 2006;7:56.
Dheda K, van Zyl Smit R, Badri M, Pai M. T-cell interferongamma release assays for the rapid immunodiagnosis of tuberculosis: clinical utility in high-burden vs. low-burden settings. Curr Opin Pulm Med 2009;15:188-200.
Pai M, Dheda K, Cunningham J, Scano F, O'Brien R. T-cell assays for the diagnosis of latent tuberculosis infection: moving the research agenda forward. Lancet Infect Dis 2007;7:428-38.
Mori T. Usefulness of interferon-gamma release assays for diagnosing TB infection and problems with these assays. J Infect Chemother 2009;15:143-55.
Andersen P, Munk ME, Pollock JM, Doherty TM. Specific immune-based diagnosis of tuberculosis. Lancet 2000;356:1099-104.
Menzies D, Pai M, Comstock G. Meta-analysis: new tests for the diagnosis of latent tuberculosis infection: areas of uncertainty and recommendations for research. Ann Intern Med 2007;146:340-54.
Diel R, Loddenkemper R, Meywald-Walter K, Niemann S, Nienhaus A. Predictive value of a whole blood IFN-gamma assay for the development of active tuberculosis disease after recent infection with Mycobacterium tuberculosis . Am J Respir Crit Care Med 2008;177:1164-70.
Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and metaanalyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
Stavri H, Ene L, Popa GL, Duiculescu D, Murgoci G, Marica C, et al. Comparison of tuberculin skin test with a whole-blood interferon gamma assay and ELISA, in HIV positive children and adolescents with TB. Roum Arch Microbiol Immunol 2009;68:14-9.
Vincenti D, Carrara S, Butera O, Bizzoni F, Casetti R, Girardi E, et al. Response to region of difference 1 (RD1) epitopes in human immunodeficiency virus (HIV)-infected individuals enrolled with suspected active tuberculosis: a pilot study. Clin Exp Immunol 2007;150:91-8.
Syed Ahamed Kabeer B, Sikhamani R, Swaminathan S, Perumal V, Paramasivam P, Raja A. Role of interferon gamma release assay in active TB diagnosis among HIV infected individuals. PLoS One 2009;4:e5718.
Idh J, Abate E, Westman A, Elias D, Janols H, Gelaw A, et al. Kinetics of the QuantiFERON-TB Gold In-Tube test during treatment of patients with sputum smear-positive tuberculosis in relation to initial TST result and severity of disease. Scand J Infect Dis 2010;42:650-7.
Tsiouris SJ, Coetzee D, Toro PL, Austin J, Stein Z, El-Sadr W. Sensitivity analysis and potential uses of a novel gamma interferon release assay for diagnosis of tuberculosis. J Clin Microbiol 2006;44:2844-50.
Raby E, Moyo M, Devendra A, Banda J, De Haas P, Ayles H, et al. The effects of HIV on the sensitivity of a whole blood IFNgamma release assay in Zambian adults with active tuberculosis. PLoS One 2008;3:e2489.
Liebeschuetz S, Bamber S, Ewer K, Deeks J, Pathan AA, Lalvani A. Diagnosis of tuberculosis in South African children with a T-cell-based assay: a prospective cohort study. Lancet 2004;364:2196-203.
Jiang W, Shao L, Zhang Y, Zhang S, Meng C, Xu Y, et al. Highsensitive and rapid detection of Mycobacterium tuberculosis infection by IFN-gamma release assay among HIVinfected individuals in BCG-vaccinated area. BMC Immunol 2009;10:31.
Davies MA, Connell T, Johannisen C, Wood K, Pienaar S, Wilkinson KA, et al. Detection of tuberculosis in HIV-infected children using an enzyme-linked immunospot assay. AIDS 2009;23:961-9.
Bourgarit A, Baron G, Breton G, Tattevin P, Katlama C, Allavena C, et al. Latent tuberculosis infection screening and 2-year outcome in antiretroviral-naive HIV-infected patients in a low-prevalence country. Ann Am Thorac Soc 2015;12:1138-45.
Luetkemeyer AF, Charlebois ED, Flores LL, Bangsberg DR, Deeks SG, Martin JN, et al. Comparison of an interferon-gamma release assay with tuberculin skin testing in HIV-infected individuals. Am J Respir Crit Care Med 2007;175:737-42.
Jones S, de Gijsel D, Wallach FR, Gurtman AC, Shi Q, Sacks H. Utility of QuantiFERON-TB Gold in-tube testing for latent TB infection in HIV-infected individuals. Int J Tuberc Lung Dis 2007;11:1190-5.
Weinfurter P, Blumberg HM, Goldbaum G, Royce R, Pang J, Tapia J, et al. Predictors of discordant tuberculin skin test and QuantiFERON(R)-TB Gold In-Tube results in various highrisk groups. Int J Tuberc Lung Dis 2011;15:1056-61.
Talati NJ, Seybold U, Humphrey B, Aina A, Tapia J, Weinfurter P, et al. Poor concordance between interferon-gamma release assays and tuberculin skin tests in diagnosis of latent tuberculosis infection among HIV-infected individuals. BMC Infect Dis 2009;9:15.
Richeldi L, Losi M, D'Amico R, Luppi M, Ferrari A, Mussini C, et al. Performance of tests for latent tuberculosis in different groups of immunocompromised patients. Chest 2009;136:198-204.
Latorre I, Martinez-Lacasa X, Font R, Lacoma A, Puig J, Tural C, et al. IFN-gamma response on T-cell based assays in HIVinfected patients for detection of tuberculosis infection. BMC Infect Dis 2010;10:348.
Santin M, Casas S, Saumoy M, Andreu A, Moure R, Alcaide F, et al. Detection of latent tuberculosis by the tuberculin skin test and a whole-blood interferon-gamma release assay, and the development of active tuberculosis in HIV-seropositive persons. Diagn Microbiol Infect Dis 2011;69:59-65.
Balcells ME, Perez CM, Chanqueo L, Lasso M, Villanueva M, Espinoza M, et al. A comparative study of two different methods for the detection of latent tuberculosis in HIV-positive individuals in Chile. Int J Infect Dis 2008;12:645-52.
Stephan C, Wolf T, Goetsch U, Bellinger O, Nisius G, Oremek G, et al. Comparing QuantiFERON-tuberculosis gold, TSPOT tuberculosis and tuberculin skin test in HIV-infected individuals from a low prevalence tuberculosis country. AIDS 2008;22:2471-9.
Hoffmann M, Reichmuth M, Fantelli K, Schoch OD, Fierz W, Furrer H, et al. Conventional tuberculin skin testing versus Tcell-based assays in the diagnosis of latent tuberculosis infection in HIV-positive patients. AIDS 2007;21:390-2.
Kimura M, Converse PJ, Astemborski J, Rothel JS, Vlahov D, Comstock GW, et al. Comparison between a whole blood interferon-gamma release assay and tuberculin skin testing for the detection of tuberculosis infection among patients at risk for tuberculosis exposure. J Infect Dis 1999;179:1297-300.
Converse PJ, Jones SL, Astemborski J, Vlahov D, Graham NM. Comparison of a tuberculin interferon-gamma assay with the tuberculin skin test in high-risk adults: effect of human immunodeficiency virus infection. J Infect Dis 1997;176:144-50.
Mathad JS, Bhosale R, Balasubramanian U, Kanade S, Mave V, Suryavanshi N, et al. Quantitative IFN-gamma and IL-2 response associated with latent tuberculosis test discordance in HIV-infected pregnant women. Am J Respir Crit Care Med 2016;193:1421-8.
Mandalakas AM, Kirchner HL, Walzl G, Gie RP, Schaaf HS, Cotton MF, et al. Optimizing the detection of recent tuberculosis infection in children in a high tuberculosis-HIV burden setting. Am J Respir Crit Care Med 2015;191:820-30.
Leidl L, Mayanja-Kizza H, Sotgiu G, Baseke J, Ernst M, Hirsch C, et al. Relationship of immunodiagnostic assays for tuberculosis and numbers of circulating CD4+ T-cells in HIV infection. Eur Respir J 2010;35:619-26.
Rangaka MX, Wilkinson KA, Seldon R, Van Cutsem G, Meintjes GA, Morroni C, et al. Effect of HIV-1 infection on TCell-based and skin test detection of tuberculosis infection. Am J Respir Crit Care Med 2007;175:514-20.
Mandalakas AM, Hesseling AC, Chegou NN, Kirchner HL, Zhu X, Marais BJ, et al. High level of discordant IGRA results in HIV-infected adults and children. Int J Tuberc Lung Dis 2008;12:417-23.
Baboolal S, Ramoutar D, Akpaka PE. Comparison of the QuantiFERON(R)-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.
Zhang M, Wang H, Liao M, Chen X, Graner M, Zhu X, et al. Diagnosis of latent tuberculosis infection in bacille Calmette-Guerin vaccinated subjects in China by interferon-gamma ELISpot assay. Int J Tuberc Lung Dis 2010;14:1556-63.
Mutsvangwa J, Millington KA, Chaka K, Mavhudzi T, Cheung YB, Mason PR, et al. Identifying recent Mycobacterium tuberculosis transmission in the setting of high HIV and TB burden. Thorax 2010;65:315-20.
Chapman AL, Munkanta M, Wilkinson KA, Pathan AA, Ewer K, Ayles H, et al. Rapid detection of active and latent tuberculosis infection in HIV-positive individuals by enumeration of Mycobacterium tuberculosis -specific T cells. AIDS 2002;16:2285-93.
Karam F, Mbow F, Fletcher H, Senghor CS, Coulibaly KD, LeFevre AM, et al. Sensitivity of IFN-gamma release assay to detect latent tuberculosis infection is retained in HIV-infected patients but dependent on HIV/AIDS progression. PLoS One 2008;3:e1441.
Huang L, Crothers K. HIV-associated opportunistic pneumonias. Respirology 2009;14:474-85.
Lee MP, Chan JW, Ng KK, Li PC. Clinical manifestations of tuberculosis in HIV-infected patients. Respirology 2000;5:423-6.
Hill PC, Jackson-Sillah DJ, Fox A, Brookes RH, de Jong BC, Lugos MD, et al. Incidence of tuberculosis and the predictive value of ELISPOT and Mantoux tests in Gambian case contacts. PLoS One 2008;3:e1379.
Bosshard V, Roux-Lombard P, Perneger T, Metzger M, Vivien R, Rochat T, et al. Do results of the T-SPOT.TB interferon-gamma release assay change after treatment of tuberculosis? Respir Med 2009;103:30-4.
Ribeiro S, Dooley K, Hackman J, Loredo C, Efron A, Chaisson RE, et al. T-SPOT.TB responses during treatment of pulmonary tuberculosis. BMC Infect Dis 2009;9:23.
Cobelens F, Borgdorff M. Boosting, BCG, and time of reading in tuberculin skin testing. Lancet 2001;358:2014.
van Zyl-Smit RN, Zwerling A, Dheda K, Pai M. Within-subject variability of interferon-g assay results for tuberculosis and boosting effect of tuberculin skin testing: a systematic review. PLoS One 2009;4:e8517.
Cattamanchi A, Ssewenyana I, Davis JL, Huang L, Worodria W, den Boon S, et al. Role of interferon-gamma release assays in the diagnosis of pulmonary tuberculosis in patients with advanced HIV infection. BMC Infect Dis 2010;10:75.
Dheda K, Chang JS, Breen RA, Haddock JA, Lipman MC, Kim LU, et al. Expression of a novel cytokine, IL-4delta2, in HIV and HIV-tuberculosis co-infection. AIDS 2005;19:1601-6.
Chen J, Zhang R, Wang J, Liu L, Zheng Y, Shen Y, et al. Interferon-gamma release assays for the diagnosis of active tuberculosis in HIV-infected patients: a systematic review and metaanalysis. PLoS One 2011;6:e26827.
Cattamanchi A, Smith R, Steingart KR, Metcalfe JZ, Date A, Coleman C, et al. Interferon-gamma release assays for the diagnosis of latent tuberculosis infection in HIV-infected individuals: a systematic review and meta-analysis. J Acquir Immune Defic Syndr 2011;56:230-8.
Santin M, Munoz L, Rigau D. Interferon-gamma release assays for the diagnosis of tuberculosis and tuberculosis infection in HIV-infected adults: a systematic review and metaanalysis. PLoS One 2012;7:e32482.
Ayubi E, Doosti-Irani A, Sanjari Moghaddam A, Sani M, Nazarzadeh M, Mostafavi E. The clinical usefulness of tuberculin skin test versus interferon-gamma release assays for diagnosis of latent tuberculosis in HIV patients: a meta-analysis. PLoS One 2016;11:e0161983.
- Downloaded
- Viewed
- 0KCI Citations
- 0WOS Citations