117
Views
0
CrossRef citations to date
0
Altmetric
Review

Current approaches for diagnosis of subclinical pulmonary tuberculosis, clinical implications and future perspectives: a scoping review

, &
Pages 715-726 | Received 12 Nov 2023, Accepted 28 Feb 2024, Published online: 05 Mar 2024

References

  • Drain PK, Bajema KL, Dowdy D, et al. Incipient and subclinical tuberculosis: a clinical review of early stages and progression of infection. Clin Microbiol Rev. 2018 Oct;31(4). doi: 10.1128/CMR.00021-18
  • Kendall EA, Shrestha S, Dowdy DW. The epidemiological importance of subclinical tuberculosis. A critical reappraisal. Am J Respir Crit Care Med. 2021;203(2):168–174.
  • Migliori GB, Ong CWM, Petrone L, et al. The definition of tuberculosis infection based on the spectrum of tuberculosis disease. Breathe (Sheff). 2021 Sep;17(3):210079.
  • Wong EB. It is time to focus on asymptomatic tuberculosis. Clin Infect Dis. 2021;72(12):e1044. doi: 10.1093/cid/ciaa1827
  • Mendelsohn SC, Fiore-Gartland A, Awany D, et al. Clinical predictors of pulmonary tuberculosis among South African adults with HIV. EClinicalMedicine. 2022 Mar;45:101328.
  • Xu Y, Cancino-Muñoz I, Torres-Puente M, et al. High-resolution mapping of tuberculosis transmission: whole genome sequencing and phylogenetic modelling of a cohort from Valencia Region, Spain. PLOS Med. 2019;16(10):e1002961. doi: 10.1371/journal.pmed.1002961
  • Emery JC, Dodd PJ, Banu S, et al. Estimating the contribution of subclinical tuberculosis disease to transmission: an individual patient data analysis from prevalence surveys. Elife. 2023 Dec 18;12:e82469. doi: 10.7554/eLife.82469
  • Zaidi SMA, Coussens AK, Seddon JA, et al. Beyond latent and active tuberculosis: a scoping review of conceptual frameworks. EClinicalMedicine. 2023 Dec;66:102332. doi: 10.1016/j.eclinm.2023.102332
  • World Health Organization. Global Tuberculosis Programme (GTB). Tuberculosis prevalence surveys: a handbook. World Health Organization; 2013.
  • Frascella B, Richards AS, Sossen B, et al. Subclinical tuberculosis disease-a review and analysis of prevalence surveys to inform definitions, burden, associations, and screening methodology. Clin Infect Dis. 2021 Aug 2;73(3):e830–e841. doi: 10.1093/cid/ciaa1402
  • Onozaki I, Law I, Sismanidis C, et al. National tuberculosis prevalence surveys in Asia, 1990-2012: an overview of results and lessons learned. Trop Med Int Health. 2015 Sep;20(9):1128–1145.
  • Min J, Chung C, Jung SS, et al. Clinical profiles of subclinical disease among pulmonary tuberculosis patients: a prospective cohort study in South Korea. BMC Pulm Med. 2020;20(1):1–9. doi: 10.1186/s12890-020-01351-z
  • Liu E, Makubi A, Drain P, et al. Tuberculosis incidence rate and risk factors among HIV-infected adults with access to antiretroviral therapy. AIDS. 2015 Jul 17;29(11):1391–1399. doi: 10.1097/QAD.0000000000000705
  • Gunasekera K, Cohen T, Gao W, et al. Smoking and HIV associated with subclinical tuberculosis: analysis of a population-based prevalence survey. Int J Tuberc Lung Dis. 2020;24(3):340–346. doi: 10.5588/ijtld.19.0387
  • Ellis PK, Martin WJ, Dodd PJ. CD4 count and tuberculosis risk in HIV-positive adults not on ART: a systematic review and meta-analysis. PeerJ. 2017;5:e4165. doi: 10.7717/peerj.4165
  • Kufa T, Mabuto T, Muchiri E, et al. Incidence of HIV-associated tuberculosis among individuals taking combination antiretroviral therapy: a systematic review and meta-analysis. PLoS One. 2014;9(11):e111209. doi: 10.1371/journal.pone.0111209
  • Oni T, Burke R, Tsekela R, et al. High prevalence of subclinical tuberculosis in HIV-1-infected persons without advanced immunodeficiency: implications for TB screening. Thorax. 2011;66(8):669–673. doi: 10.1136/thx.2011.160168
  • Riou C, Du Bruyn E, Stek C, et al. Relationship of SARS-CoV-2–specific CD4 response to COVID-19 severity and impact of HIV-1 and tuberculosis coinfection. J Clin Investig. 2021;131(12). doi: 10.1172/JCI149125
  • Ledesma JR, Ma J, Zheng P, et al. Interferon-gamma release assay levels and risk of progression to active tuberculosis: a systematic review and dose-response meta-regression analysis. BMC Infect Dis. 2021 May 22;21(1):467. doi: 10.1186/s12879-021-06141-4
  • Singer SN, Ndumnego OC, Kim RS, et al. Plasma host protein biomarkers correlating with increasing mycobacterium tuberculosis infection activity prior to tuberculosis diagnosis in people living with HIV. EBioMedicine. 2022 Jan;75:103787.
  • Wang Z, Li H, Song S, et al. Transmission of tuberculosis in an incarcerated population during the subclinical period: a cross-sectional study in Qingdao, China. Front Public Health. 2023;11:1098519. doi: 10.3389/fpubh.2023.1098519
  • Organization WH. Global tuberculosis report 2021: supplementary material. 2022.
  • Bayaa R, Ndiaye MDB, Chedid C, et al. Multi-country evaluation of RISK6, a 6-gene blood transcriptomic signature, for tuberculosis diagnosis and treatment monitoring. Sci Rep. 2021 Jul 1;11(1):13646. doi: 10.1038/s41598-021-93059-1
  • Roya-Pabon CL, Perez-Velez CM. Tuberculosis exposure, infection and disease in children: a systematic diagnostic approach. Pneumonia (Nathan). 2016;8(1):23. doi: 10.1186/s41479-016-0023-9
  • Gill CM, Dolan L, Piggott LM, et al. New developments in tuberculosis diagnosis and treatment. Breathe (Sheff). 2022 Mar;18(1):210149.
  • World Health Organization. Automated real-time nucleic acid amplification technology for rapid and simultaneous detection of tuberculosis and rifampicin resistance: xpert MTB. Policy update ed. World Health Organization; 2013.
  • Nikam C, Jagannath M, Narayanan MM, et al. Rapid diagnosis of Mycobacterium tuberculosis with Truenat MTB: a near-care approach. PLoS One. 2013;8(1):e51121. doi: 10.1371/journal.pone.0051121
  • Cantera JL, Lillis LM, Peck RB, et al. Performance of novel antibodies for lipoarabinomannan to develop diagnostic tests for Mycobacterium tuberculosis. PLoS One. 2022;17(9):e0274415. doi: 10.1371/journal.pone.0274415
  • Shapiro AE, Olson AM, Kidoguchi L, et al. Complementary nonsputum diagnostic testing for tuberculosis in people with HIV using oral swab PCR and urine lipoarabinomannan detection. J Clin Microbiol. 2022 Aug 17;60(8):e0043122. doi: 10.1128/jcm.00431-22
  • Shah M, Hanrahan C, Wang ZY, et al. Lateral flow urine lipoarabinomannan assay for detecting active tuberculosis in HIV-positive adults. Cochrane Database Syst Rev. 2016 May 10;2016(5):Cd011420. doi: 10.1002/14651858.CD011420.pub2
  • Székely R, Sossen B, Mukoka M, et al. Multicentre accuracy trial of FUJIFILM SILVAMP TB LAM test in people with HIV reveals lot variability. medRxiv. 2022 Sep 9;22278961. doi: 10.1101/2022.09.07.22278961
  • Yu G, Shen Y, Ye B, et al. Diagnostic accuracy of Mycobacterium tuberculosis cell-free DNA for tuberculosis: a systematic review and meta-analysis. PLoS One. 2021;16(6):e0253658. doi: 10.1371/journal.pone.0253658
  • Oreskovic A, Panpradist N, Marangu D, et al. Diagnosing pulmonary tuberculosis by using sequence-specific purification of urine cell-free DNA. J Clin Microbiol. 2021 Jul 19;59(8):e0007421. doi: 10.1128/JCM.00074-21
  • Keer JT, Birch L. Molecular methods for the assessment of bacterial viability. J Microbiol Methods. 2003 May;53(2):175–183. doi: 10.1016/S0167-7012(03)00025-3
  • Lu J, Zheng H, Chu P, et al. Direct detection from clinical sputum samples to differentiate live and dead Mycobacterium Tuberculosis. J Clin Lab Anal. 2019 Mar;33(3):e22716.
  • Barr DA, Omollo C, Mason M, et al. Flow cytometry method for absolute counting and single-cell phenotyping of mycobacteria. Sci Rep. 2021 Sep 20;11(1):18661. doi: 10.1038/s41598-021-98176-5
  • Babin BM, Fernandez-Cuervo G, Sheng J, et al. Chemiluminescent protease probe for rapid, sensitive, and inexpensive detection of live mycobacterium tuberculosis. ACS Cent Sci. 2021 May 26;7(5):803–814. doi: 10.1021/acscentsci.0c01345
  • Walter ND, Born SEM, Robertson GT, et al. Mycobacterium tuberculosis precursor rRNA as a measure of treatment-shortening activity of drugs and regimens. Nat Commun. 2021 May 18;12(1):2899. doi: 10.1038/s41467-021-22833-6
  • Rogers GB, Stressmann FA, Koller G, et al. Assessing the diagnostic importance of nonviable bacterial cells in respiratory infections. Diagn Microbiol Infect Dis. 2008 Oct;62(2):133–141.
  • Dorn-In S, Gareis M, Schwaiger K. Differentiation of live and dead mycobacterium tuberculosis complex in meat samples using PMA qPCR. Food Microbiol. 2019 Dec;84:103275. doi: 10.1016/j.fm.2019.103275
  • Nikolayevskyy V, Miotto P, Pimkina E, et al. Utility of propidium monoazide viability assay as a biomarker for a tuberculosis disease. Tuberculosis (Edinb). 2015 Mar;95(2):179–185.
  • Seiler P, Ulrichs T, Bandermann S, et al. Cell-wall alterations as an attribute of mycobacterium tuberculosis in latent infection. J Infect Dis. 2023 Nov 1;188(9):1326–1331. doi: 10.1086/378563
  • Alebouyeh S, Weinrick B, Achkar JM, et al. Feasibility of novel approaches to detect viable mycobacterium tuberculosis within the spectrum of the tuberculosis disease. Front Med. 2022;9:965359. doi: 10.3389/fmed.2022.965359
  • Heyckendorf J, Gillespie SH, Ruhwald M. Culture-free proof of mycobacterium tuberculosis - a new assay for viable bacteria. EBioMedicine. 2020 Dec;62:103117. doi: 10.1016/j.ebiom.2020.103117
  • Wang WH, Takeuchi R, Jain SH, et al. A novel, rapid (within hours) culture-free diagnostic method for detecting live mycobacterium tuberculosis with high sensitivity. EBioMedicine. 2020 Oct;60:103007.
  • Rauhut R, Klug G. mRNA degradation in bacteria. FEMS Microbiol Rev. 1999 Jun;23(3):353–370. doi: 10.1111/j.1574-6976.1999.tb00404.x
  • Weigel KM, Jones KL, Do JS, et al. Molecular viability testing of bacterial pathogens from a complex human sample matrix. PLoS One. 2013;8(1):e54886. doi: 10.1371/journal.pone.0054886
  • Cubero N, Esteban J, Palenque E, et al. Evaluation of the detection of mycobacterium tuberculosis with metabolic activity in culture-negative human clinical samples. Clin Microbiol Infect. 2013 Mar;19(3):273–278.
  • Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005 Nov 15;19(22):2645–2655. doi: 10.1101/gad.1299905
  • Prados-Rosales R, Baena A, Martinez LR, et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest. 2011 Apr;121(4):1471–1483.
  • Schirmer S, Rauh L, Alebouyeh S, et al. Immunogenicity of mycobacterial extracellular vesicles isolated from host-related conditions informs about tuberculosis disease status. Front Microbiol. 2022;13:907296. doi: 10.3389/fmicb.2022.907296
  • Zheng W, LaCourse SM, Song B, et al. Diagnosis of paediatric tuberculosis by optically detecting two virulence factors on extracellular vesicles in blood samples. Nat Biomed Eng. 2022 Aug;6(8):979–991.
  • Kumar S, Gopinathan R, Chandra GK, et al. Rapid detection of bacterial infection and viability assessment with high specificity and sensitivity using raman microspectroscopy. Anal Bioanal Chem. 2020 Apr;412(11):2505–2516.
  • Mamishi S, Pourakbari B, Marjani M, et al. Diagnosis of latent tuberculosis infection among immunodeficient individuals: review of concordance between interferon-gamma release assays and the tuberculin skin test. Br J Biomed Sci. 2014;71(3):115–124. doi: 10.1080/09674845.2014.11669976
  • Pourakbari B, Mamishi S, Marjani M, et al. Novel T-cell assays for the discrimination of active and latent tuberculosis infection: the diagnostic value of PPE family. Mol Diagn Ther. 2015 Oct;19(5):309–316.
  • Pourakbari B, Mamishi S, Benvari S, et al. Comparison of the QuantiFERON-TB gold plus and QuantiFERON-TB gold in-tube interferon-γ release assays: a systematic review and meta-analysis. Adv Med Sci. 2019 Sep;64(2):437–443.
  • Rezaei N, Hosseini N-S, Saghazadeh A, et al. Tuberculosis: integrated studies for a complex disease 2050. Tuberculosis: integrated studies for a complex disease. Springer International Publishing; 2023. p. 1063–1098.
  • Mahmoudi S, Pourakbari B, Mamishi S. Immunodiagnostics of tuberculosis: recent discoveries. Tuberculosis: integrated studies for a complex disease. Springer International Publishing; 2023. p. 139–150.
  • Andrews JR, Nemes E, Tameris M, et al. Serial QuantiFERON testing and tuberculosis disease risk among young children: an observational cohort study. Lancet Respir Med. 2017 Apr;5(4):282–290.
  • Li Q, Ren W, Yuan J, et al. Significant difference in Th1/Th2 paradigm induced by tuberculosis-specific antigens between IGRA-positive and IGRA-negative patients. Front Immunol. 2022;13:904308. doi: 10.3389/fimmu.2022.904308
  • Scriba TJ, Penn-Nicholson A, Shankar S, et al. Sequential inflammatory processes define human progression from M. tuberculosis infection to tuberculosis disease. PLOS Pathog. 2017 Nov;13(11):e1006687.
  • Delogu G, Chiacchio T, Vanini V, et al. Methylated HBHA produced in M. smegmatis discriminates between active and non-active tuberculosis disease among RD1-responders. PLoS One. 2011 Mar 29;6(3):e18315. doi: 10.1371/journal.pone.0018315
  • Chiacchio T, Delogu G, Vanini V, et al. Immune characterization of the HBHA-specific response in mycobacterium tuberculosis-infected patients with or without HIV infection. PLoS One. 2017;12(8):e0183846. doi: 10.1371/journal.pone.0183846
  • Tang J, Huang Y, Cai Z, et al. Mycobacterial heparin-binding hemagglutinin (HBHA)-induced interferon-γ release assay (IGRA) for discrimination of latent and active tuberculosis: a systematic review and meta-analysis. PLoS One. 2021;16(7):e0254571. doi: 10.1371/journal.pone.0254571
  • Mamishi S, Mahmoudi S, Banar M, et al. Diagnostic accuracy of interferon (IFN)-γ inducible protein 10 (IP-10) as a biomarker for the discrimination of active and latent tuberculosis. Mol Biol Rep. 2019 Dec;46(6):6263–6269.
  • Mamishi S, Pourakbari B, Sadeghi RH, et al. Diagnostic accuracy of monocyte chemotactic protein (MCP)-2 as biomarker in response to PE35/PPE68 proteins: a promising diagnostic method for the discrimination of active and latent tuberculosis. Protein Pept Lett. 2019;26(4):281–286. doi: 10.2174/0929866526666190119165805
  • Mamishi S, Pourakbari B, Shams H, et al. Improving T-cell assays for diagnosis of latent TB infection: confirmation of the potential role of testing interleukin-2 release in Iranian patients. Allergol Immunopathol (Madr). 2016 Jul;44(4):314–321
  • Mamishi S, Pourakbari B, Marjani M, et al. Discriminating between latent and active tuberculosis: the role of interleukin-2 as biomarker. J Infect. 2015 Apr;70(4):429–431.
  • Tanner R, O’Shea MK, Fletcher HA, et al. In vitro mycobacterial growth inhibition assays: a tool for the assessment of protective immunity and evaluation of tuberculosis vaccine efficacy. Vaccine. 2016 Sep 7;34(39):4656–4665. doi: 10.1016/j.vaccine.2016.07.058
  • O’Shea MK, Tanner R, Müller J, et al. Immunological correlates of mycobacterial growth inhibition describe a spectrum of tuberculosis infection. Sci Rep. 2018 Sep 27;8(1):14480. doi: 10.1038/s41598-018-32755-x
  • Lee H, Kim J, Kang YA, et al. In vitro mycobacterial growth inhibition in South Korean adults with latent TB infection. Front Immunol. 2019;10:896. doi: 10.3389/fimmu.2019.00896
  • Tabone O, Verma R, Singhania A, et al. Blood transcriptomics reveal the evolution and resolution of the immune response in tuberculosis. J Exp Med. 2021 Oct 4;218(10). doi: 10.1084/jem.20210915
  • Esmail H, Lai RP, Lesosky M, et al. Complement pathway gene activation and rising circulating immune complexes characterize early disease in HIV-associated tuberculosis. Proc Natl Acad Sci U S A. 2018 Jan 30;115(5):E964–e973. doi: 10.1073/pnas.1711853115
  • Achkar JM, Cortes L, Croteau P, et al. Host protein biomarkers identify active tuberculosis in HIV uninfected and Co-infected individuals. EBioMedicine. 2015 Sep;2(9):1160–1168.
  • Bark CM, Manceur AM, Malone LL, et al. Identification of host proteins predictive of early stage mycobacterium tuberculosis infection. EBioMedicine. 2017 Jul;21:150–157.
  • Morris TC, Hoggart CJ, Chegou NN, et al. Evaluation of host serum protein biomarkers of tuberculosis in sub-saharan Africa. Front Immunol. 2021;12:639174. doi: 10.3389/fimmu.2021.639174
  • Zak DE, Penn-Nicholson A, Scriba TJ, et al. A blood RNA signature for tuberculosis disease risk: a prospective cohort study. Lancet. 2016 Jun 4;387(10035):2312–2322. doi: 10.1016/S0140-6736(15)01316-1
  • Warsinske HC, Rao AM, Moreira FMF, et al. Assessment of validity of a blood-based 3-gene signature score for progression and diagnosis of tuberculosis, disease severity, and treatment response. JAMA Netw Open. 2018 Oct 5;1(6):e183779. doi: 10.1001/jamanetworkopen.2018.3779
  • Penn-Nicholson A, Hraha T, Thompson EG, et al. Discovery and validation of a prognostic proteomic signature for tuberculosis progression: a prospective cohort study. PLOS Med. 2019 Apr;16(4):e1002781.
  • MacPherson P, Webb EL, Lalloo DG, et al. Design and protocol for a pragmatic randomised study to optimise screening, prevention and care for tuberculosis and HIV in Malawi (PROSPECT study). Wellcome Open Res. 2018;3:3. doi: 10.12688/wellcomeopenres.14598.3
  • Long R, Lau A, Barrie J, et al. Limitations of chest radiography in diagnosing subclinical pulmonary tuberculosis in Canada. Mayo Clin Proc Innov Qual Outcomes. 2023 Jun;7(3):165–170.
  • Tang P, Liang E, Zhang X, et al. Prevalence and risk factors of subclinical tuberculosis in a low-incidence setting in China. Front Microbiol. 2022;12:4056. doi: 10.3389/fmicb.2021.731532
  • Patterson B, Wood R. Is cough really necessary for TB transmission? Tuberculosis. 2019;117:31–35. doi: 10.1016/j.tube.2019.05.003
  • Behr M, Warren S, Salamon H, et al. Transmission of mycobacterium tuberculosis from patients smear-negative for acid-fast bacilli. Lancet. 1999;353(9151):444–449. doi: 10.1016/S0140-6736(98)03406-0
  • Jiménez-Corona ME, García-García L, DeRiemer K, et al. Gender differentials of pulmonary tuberculosis transmission and reactivation in an endemic area. Thorax. 2006 Apr;61(4):348–353.
  • Coleman M, Martinez L, Theron G, et al. Mycobacterium tuberculosis transmission in high-incidence settings—new paradigms and insights. Pathogens. 2022 Oct 25;11(11):1228. doi: 10.3390/pathogens11111228
  • Vaezipour N, Fritschi N, Brasier N, et al. Towards accurate point-of-care tests for tuberculosis in children. Pathogens. 2022 Mar 8;11(3):327. doi: 10.3390/pathogens11030327
  • Fritschi N, Wind A, Hammer J, et al. Subclinical tuberculosis in children: diagnostic strategies for identification reported in a 6-year national prospective surveillance study. Clin Infect Dis. 2022 Mar 1;74(4):678–684. doi: 10.1093/cid/ciab708
  • Unterweger M, Götzinger F, Bogyi M, et al. Childhood tuberculosis in Vienna between 2010 and 2016. Wien Klin Wochenschr. 2019 Aug;131(15–16):356–361.
  • Ziemele B, Ranka R, Ozere I. Pediatric and adolescent tuberculosis in Latvia, 2011-2014: case detection, diagnosis and treatment. Int J Tuberc Lung Dis. 2017 Jun 1;21(6):637–645. doi: 10.5588/ijtld.16.0270
  • Dorjee K, Topgyal S, Dorjee C, et al. High prevalence of active and latent tuberculosis in children and adolescents in Tibetan schools in India: the zero TB kids initiative in Tibetan refugee children. Clin Infect Dis. 2019 Aug 16;69(5):760–768. doi: 10.1093/cid/ciy987
  • Laniado-Laborín R. Clinical challenges in the era of multiple and extensively drug-resistant tuberculosis. Rev Panam Salud Publica. 2017;41:e167. doi: 10.26633/RPSP.2017.167
  • Naidoo K, Moodley MC, Hassan-Moosa R, et al. Recurrent subclinical tuberculosis among antiretroviral therapy–accessing participants: incidence, clinical course, and outcomes. Clinl Infect Dis. 2022;75(9):1628–1636. doi: 10.1093/cid/ciac185
  • Kendall EA, Fofana MO, Dowdy DW. Burden of transmitted multidrug resistance in epidemics of tuberculosis: a transmission modelling analysis. Lancet Respir Med. 2015 Dec;3(12):963–972. doi: 10.1016/S2213-2600(15)00458-0
  • Nathavitharana RR, Garcia-Basteiro AL, Ruhwald M, et al. Reimagining the status quo: how close are we to rapid sputum-free tuberculosis diagnostics for all? EBioMedicine. 2022 Apr;78:103939.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.