We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Medicine AI
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Diagnostic value of nucleic acid amplification tests for tuberculous pleural effusion

    Xu-Hui Wen

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    Department of Parasitology, Basic Medical Sciences College of Inner Mongolia Medical University, Hohhot, 010050, China

    ,
    Yu-Ling Han

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    Department of Parasitology, Basic Medical Sciences College of Inner Mongolia Medical University, Hohhot, 010050, China

    ,
    Xi-Shan Cao

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    ,
    Wen Zhao

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    ,
    Zhi Yan

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    Department of Parasitology, Basic Medical Sciences College of Inner Mongolia Medical University, Hohhot, 010050, China

    ,
    Li Yan

    Department of Respiratory & Critical Care Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    ,
    Jian-Xun Wen

    Department of Medical Experiment Center, Basic Medical Sciences College of Inner Mongolia Medical University, Hohhot, 010050, China

    ,
    Zhi-De Hu

    *Author for correspondence:

    E-mail Address: hzdlj81@163.com

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    &
    Wen-Qi Zheng

    **Author for correspondence:

    E-mail Address: zhengwenqi2011@163.com

    Department of Laboratory Medicine, the Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010010, China

    Department of Parasitology, Basic Medical Sciences College of Inner Mongolia Medical University, Hohhot, 010050, China

    Published Online:https://doi.org/10.2217/fmb-2023-0025

    Diagnosing tuberculous pleural effusion (TPE) is challenging for pulmonologists and laboratory scientists. The gold standards for TPE diagnosis are pleural fluid Ziehl–Neelsen staining, Mycobacterium tuberculosis (Mtb) culture and pleural biopsy. These tools have limitations, including low sensitivity, long turnaround time and invasiveness. The nucleic acid amplification test (NAAT) is a rapid and minimally invasive tool for diagnosing TPE. This review summarizes the diagnostic accuracy of available NAATs for TPE, with a focus on the evidence from systematic reviews and meta-analyses. The NAATs summarized in this review include in-house NAATs, GeneXpert-MTB/RIF, GeneXpert-MTB/RIF Ultra, simultaneous amplification and testing–tuberculosis, FluoroType MTB and loop-mediated isothermal amplification.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1. Global Tuberculosis Report. WHO, Geneva, Switzerland (2021).
    • 2. Global Tuberculosis Report. WHO, Geneva, Switzerland (2020).
    • 3. Light RW. Update on tuberculous pleural effusion. Respirology 15(3), 451–458 (2010).
    • 4. Tyagi S, Sharma N, Tyagi JS, Haldar S. Challenges in pleural tuberculosis diagnosis: existing reference standards and nucleic acid tests. Future Microbiol. 12, 1201–1218 (2017). •• This is a comprehensive meta-analysis investigating the diagnostic accuracy of the nucleic acid amplification test for tuberculous pleural effusion.
    • 5. Bielsa S, Acosta C, Pardina M, Civit C, Porcel JM. Tuberculous pleural effusion: clinical characteristics of 320 patients. Arch. Bronconeumol. (Engl. Ed.) 55(1), 17–22 (2019).
    • 6. Trajman A, Pai M, Dheda K et al. Novel tests for diagnosing tuberculous pleural effusion: what works and what does not? Eur. Respir. J. 31(5), 1098–1106 (2008).
    • 7. Brisson-Noel A, Aznar C, Chureau C et al. Diagnosis of tuberculosis by DNA amplification in clinical practice evaluation. Lancet 338(8763), 364–366 (1991).
    • 8. Jungkind D. Tech.Sight. Molecular testing for infectious disease. Science 294(5546), 1553–1555 (2001).
    • 9. Louie M, Louie L, Simor AE. The role of DNA amplification technology in the diagnosis of infectious diseases. CMAJ 163(3), 301–309 (2000).
    • 10. Pao CC, Yen TS, You JB, Maa JS, Fiss EH, Chang CH. Detection and identification of Mycobacterium tuberculosis by DNA amplification. J. Clin. Microbiol. 28(9), 1877–1880 (1990).
    • 11. Gallo JF, Pinhata JM, Chimara E, Gonçalves MG, Fukasawa LO, Oliveira RS. Performance of an in-house real-time polymerase chain reaction for identification of Mycobacterium tuberculosis isolates in laboratory routine diagnosis from a high burden setting. Mem Inst Oswaldo Cruz 111(9), 545–550 (2016).
    • 12. Miller MB, Popowitch EB, Backlund MG, Ager EP. Performance of Xpert MTB/RIF RUO assay and IS6110 real-time PCR for Mycobacterium tuberculosis detection in clinical samples. J. Clin. Microbiol. 49(10), 3458–3462 (2011).
    • 13. Villegas MV, Labrada LA, Saravia NG. Evaluation of polymerase chain reaction, adenosine deaminase, and interferon-gamma in pleural fluid for the differential diagnosis of pleural tuberculosis. Chest 118(5), 1355–1364 (2000).
    • 14. Pai M, Flores LL, Hubbard A, Riley LW, Colford JM Jr. Nucleic acid amplification tests in the diagnosis of tuberculous pleuritis: a systematic review and meta-analysis. BMC Infect. Dis. 4, 6 (2004).
    • 15. Che N, Yang X, Liu Z, Li K, Chen X. Rapid detection of cell-free Mycobacterium tuberculosis DNA in tuberculous pleural effusion. J. Clin. Microbiol. 55(5), 1526–1532 (2017).
    • 16. Yang X, Che N, Duan H et al. Cell-free Mycobacterium tuberculosis DNA test in pleural effusion for tuberculous pleurisy: a diagnostic accuracy study. Clin. Microbiol. Infect. 26(8), 1089.e1081–1089.e1086 (2020).
    • 17. Takagi N, Hasegawa Y, Ichiyama S, Shibagaki T, Shimokata K. Polymerase chain reaction of pleural biopsy specimens for rapid diagnosis of tuberculous pleuritis. Int. J. Tuberc. Lung Dis. 2(4), 338–341 (1998).
    • 18. Hasaneen NA, Zaki ME, Shalaby HM, El-Morsi AS. Polymerase chain reaction of pleural biopsy is a rapid and sensitive method for the diagnosis of tuberculous pleural effusion. Chest 124(6), 2105–2111 (2003).
    • 19. Amer S, Hefnawy AE, Wahab NA, Okasha H, Baz A. Evaluation of different laboratory methods for rapid diagnosis of tuberculous pleurisy. Int. J. Mycobacteriol. 5(4), 437–445 (2016).
    • 20. Li L, Wang Y, Zhang R et al. Diagnostic value of polymerase chain reaction/acid-fast bacilli in conjunction with computed tomography-guided pleural biopsy in tuberculous pleurisy: a diagnostic accuracy study. Medicine (Baltimore) 98(29), e15992 (2019).
    • 21. Wang Z, Xu LL, Wu YB et al. Diagnostic value and safety of medical thoracoscopy in tuberculous pleural effusion. Respir. Med. 109(9), 1188–1192 (2015).
    • 22. Lima DM, Colares JK, Da Fonseca BA. Combined use of the polymerase chain reaction and detection of adenosine deaminase activity on pleural fluid improves the rate of diagnosis of pleural tuberculosis. Chest 124(3), 909–914 (2003).
    • 23. Michos AG, Daikos GL, Tzanetou K et al. Detection of Mycobacterium tuberculosis DNA in respiratory and nonrespiratory specimens by the Amplicor MTB PCR. Diagn. Microbiol. Infect. Dis. 54(2), 121–126 (2006).
    • 24. Kalantri Y, Hemvani N, Chitnis DS. Evaluation of real-time polymerase chain reaction, interferon-gamma, adenosine deaminase, and immunoglobulin A for the efficient diagnosis of pleural tuberculosis. Int. J. Infect. Dis. 15(4), e226–e231 (2011).
    • 25. Sankar S, Kuppanan S, Balakrishnan B, Nandagopal B. Analysis of sequence diversity among IS6110 sequence of Mycobacterium tuberculosis: possible implications for PCR based detection. Bioinformation 6(7), 283–285 (2011).
    • 26. Tadele A, Beyene D, Hussein J et al. Immunocytochemical detection of Mycobacterium tuberculosis complex specific antigen, MPT64, improves diagnosis of tuberculous lymphadenitis and tuberculous pleuritis. BMC Infect. Dis. 14, 585 (2014).
    • 27. Khosravi AD, Alami A, Meghdadi H, Hosseini AA. Identification of Mycobacterium tuberculosis in clinical specimens of patients suspected of having extrapulmonary tuberculosis by application of nested PCR on five different genes. Front. Cell. Infect. Microbiol. 7, 3 (2017).
    • 28. Chakravorty S, Sen MK, Tyagi JS. Diagnosis of extrapulmonary tuberculosis by smear, culture, and PCR using universal sample processing technology. J. Clin. Microbiol. 43(9), 4357–4362 (2005).
    • 29. Raj A, Singh N, Gupta KB et al. Comparative evaluation of several gene targets for designing a multiplex-PCR for an early diagnosis of extrapulmonary tuberculosis. Yonsei Med. J. 57(1), 88–96 (2016).
    • 30. Rafi W, Venkataswamy MM, Ravi V, Chandramuki A. Rapid diagnosis of tuberculous meningitis: a comparative evaluation of in-house PCR assays involving three mycobacterial DNA sequences, IS6110, MPB-64 and 65 kDa antigen. J. Neurol. Sci. 252(2), 163–168 (2007).
    • 31. Ginesu F, Pirina P, Sechi LA et al. Microbiological diagnosis of tuberculosis: a comparison of old and new methods. J. Chemother. 10(4), 295–300 (1998).
    • 32. Gill MK, Kukreja S, Chhabra N. Evaluation of nested polymerase chain reaction for rapid diagnosis of clinically suspected tuberculous pleurisy. J. Clin. Diagn. Res. 7(11), 2456–2458 (2013).
    • 33. Gao Y, Ou Q, Huang F et al. Improved diagnostic power by combined interferon-gamma release assay and nested-PCR in tuberculous pleurisy in high tuberculosis prevalence area. FEMS Immunol. Med. Microbiol. 66(3), 393–398 (2012).
    • 34. Kuwano K, Minamide W, Kusunoki S et al. Evaluation of nested polymerase chain reaction for detecting mycobacterial DNA in pleural fluid. Kansenshogaku Zasshi 69(2), 175–180 (1995).
    • 35. Reechaipichitkul W, Lulitanond V, Sungkeeree S, Patjanasoontorn B. Rapid diagnosis of tuberculous pleural effusion using polymerase chain reaction. Southeast Asian J. Trop. Med. Public Health 31(3), 509–514 (2000).
    • 36. Mustafa T, Wergeland I, Baba K, Pathak S, Hoosen AA, Dyrhol-Riise AM. Mycobacterial antigens in pleural fluid mononuclear cells to diagnose pleural tuberculosis in HIV co-infected patients. BMC Infect. Dis. 20(1), 459 (2020).
    • 37. Liu KT, Su WJ, Perng RP. Clinical utility of polymerase chain reaction for diagnosis of smear-negative pleural tuberculosis. J. Chin. Med. Assoc. 70(4), 148–151 (2007).
    • 38. Montenegro LM, Silva BC, Lima JF et al. The performance of an in-house nested-PCR technique for pleural tuberculosis diagnoses. Rev. Soc. Bras. Med. Trop. 46(5), 594–599 (2013).
    • 39. Yum HK, Choi SJ. Detection of mycobacterial DNA using nested polymerase chain reaction of pleural biopsy specimens: compared to pathologic findings. Korean J. Intern. Med. 18(2), 89–93 (2003).
    • 40. Sharma S, Dahiya B, Sreenivas V et al. Comparative evaluation of GeneXpert MTB/RIF and multiplex PCR targeting mpb64 and IS6110 for the diagnosis of pleural TB. Future Microbiol. 13, 407–413 (2018).
    • 41. Bandyopadhyay D, Gupta S, Banerjee S et al. Adenosine deaminase estimation and multiplex polymerase chain reaction in diagnosis of extra-pulmonary tuberculosis. Int. J. Tuberc. Lung Dis. 12(10), 1203–1208 (2008).
    • 42. Ehlers S, Ignatius R, Regnath T, Hahn H. Diagnosis of extrapulmonary tuberculosis by Gen-Probe amplified Mycobacterium tuberculosis direct test. J. Clin. Microbiol. 34(9), 2275–2279 (1996).
    • 43. Rantakokko-Jalava K, Marjamäki M, Marttila H, Mäkelä L, Valtonen V, Viljanen MK. LCx Mycobacterium tuberculosis assay is valuable with respiratory specimens, but provides little help in the diagnosis of extrapulmonary tuberculosis. Ann. Med. 33(1), 55–62 (2001).
    • 44. Irfan M, Idrees F, Jabeen K, Zubairi ABS, Butt S, Hasan R. Accuracy of genotype MTBDRplus line probe assay in patients with tuberculous pleural effusion: comparison with clinical and culture based diagnosis. Infect. Dis. (Lond.) 52(4), 235–241 (2020).
    • 45. Mitarai S, Shishido H, Kurashima A, Tamura A, Nagai H. Comparative study of amplicor Mycobacterium PCR and conventional methods for the diagnosis of pleuritis caused by mycobacterial infection. Int. J. Tuberc. Lung Dis. 4(9), 871–876 (2000).
    • 46. Horita N, Yamamoto M, Sato T et al. Sensitivity and specificity of Cobas TaqMan MTB real-time polymerase chain reaction for culture-proven Mycobacterium tuberculosis: meta-analysis of 26999 specimens from 17 studies. Sci. Rep. 5, 18113 (2015).
    • 47. Ling DI, Flores LL, Riley LW, Pai M. Commercial nucleic-acid amplification tests for diagnosis of pulmonary tuberculosis in respiratory specimens: meta-analysis and meta-regression. PLOS ONE 3(2), e1536 (2008).
    • 48. Steingart KR, Sohn H, Schiller I et al. Xpert® MTB/RIF assay for pulmonary tuberculosis and rifampicin resistance in adults. Cochrane Database Syst. Rev. (1), CD009593 (2013).
    • 49. Automated Real-Time Nucleic Acid Amplification Technology for Rapid and Simultaneous Detection of Tuberculosis and Rifampicin Resistance: Xpert MTB/RIF Assay for the Diagnosis of Pulmonary and Extrapulmonary TB in Adults and Children: Policy Update. WHO, Geneva, Switzerland (2013).
    • 50. Zifodya JS, Kreniske JS, Schiller I et al. Xpert Ultra versus Xpert MTB/RIF for pulmonary tuberculosis and rifampicin resistance in adults with presumptive pulmonary tuberculosis. Cochrane Database Syst. Rev. 2, CD009593 (2021).
    • 51. Yu G, Zhong F, Ye B, Xu X, Chen D, Shen Y. Diagnostic accuracy of the Xpert MTB/RIF assay for lymph node tuberculosis: a systematic review and meta-analysis. Biomed. Res. Int. 2019, 4878240 (2019).
    • 52. Hernandez AV, De Laurentis L, Souza I et al. Diagnostic accuracy of Xpert MTB/RIF for tuberculous meningitis: systematic review and meta-analysis. Trop. Med. Int. Health 26(2), 122–132 (2021).
    • 53. Maynard-Smith L, Larke N, Peters JA, Lawn SD. Diagnostic accuracy of the Xpert MTB/RIF assay for extrapulmonary and pulmonary tuberculosis when testing non-respiratory samples: a systematic review. BMC Infect. Dis. 14, 709 (2014).
    • 54. Denkinger CM, Schumacher SG, Boehme CC, Dendukuri N, Pai M, Steingart KR. Xpert MTB/RIF assay for the diagnosis of extrapulmonary tuberculosis: a systematic review and meta-analysis. Eur. Respir. J. 44(2), 435–446 (2014).
    • 55. Sehgal IS, Dhooria S, Aggarwal AN, Behera D, Agarwal R. Diagnostic performance of Xpert MTB/RIF in tuberculous pleural effusion: systematic review and meta-analysis. J. Clin. Microbiol. 54(4), 1133–1136 (2016).
    • 56. Kohli M, Schiller I, Dendukuri N et al. Xpert® MTB/RIF assay for extrapulmonary tuberculosis and rifampicin resistance. Cochrane Database Syst. Rev. 8, CD012768 (2018).
    • 57. Kohli M, Schiller I, Dendukuri N et al. Xpert MTB/RIF Ultra and Xpert MTB/RIF assays for extrapulmonary tuberculosis and rifampicin resistance in adults. Cochrane Database Syst. Rev. 1, CD012768 (2021).
    • 58. Yu W, Shen Y, Zhu P, Chen D. Head-to-head comparison of the efficacy of Xpert MTB/RIF Ultra and Xpert MTB/RIF for the diagnosis of tuberculous pleurisy: a systematic review and meta-analysis. Medicine (Baltimore) 101(20), e29363 (2022). • This systematic review and meta-analysis compares the diagnostic accuracy of GeneXpert-MTB/RIF Ultra and GeneXpert-MTB/RIF in head-to-head manner.
    • 59. Tortoli E, Russo C, Piersimoni C et al. Clinical validation of Xpert MTB/RIF for the diagnosis of extrapulmonary tuberculosis. Eur. Respir. J. 40(2), 442–447 (2012).
    • 60. Kim YW, Kwak N, Seong MW et al. Accuracy of the Xpert® MTB/RIF assay for the diagnosis of extra-pulmonary tuberculosis in South Korea. Int. J. Tuberc. Lung Dis. 19(1), 81–86 (2015).
    • 61. Penz E, Boffa J, Roberts DJ et al. Diagnostic accuracy of the Xpert® MTB/RIF assay for extra-pulmonary tuberculosis: a meta-analysis. Int. J. Tuberc. Lung Dis. 19(3), 278–284 i–iii (2015).
    • 62. Huo ZY, Peng L. Is Xpert MTB/RIF appropriate for diagnosing tuberculous pleurisy with pleural fluid samples? A systematic review. BMC Infect. Dis. 18(1), 284 (2018).
    • 63. Qiu YR, Chen YY, Wu XR et al. Accuracy of Xpert MTB/RIF assay for the diagnosis of tuberculous pleural effusion. J. Clin. Lab. Anal. 36(1), e24185 (2021).
    • 64. Jiang J, Yang J, Shi Y et al. Head-to-head comparison of the diagnostic accuracy of Xpert MTB/RIF and Xpert MTB/RIF Ultra for tuberculosis: a meta-analysis. Infect. Dis. (Lond.) 52(11), 763–775 (2020).
    • 65. Christopher DJ, Schumacher SG, Michael JS et al. Performance of Xpert MTB/RIF on pleural tissue for the diagnosis of pleural tuberculosis. Eur. Respir. J. 42(5), 1427–1429 (2013).
    • 66. Sun W, Zhou Y, Li W et al. Diagnostic yield of Xpert MTB/RIF on contrast-enhanced ultrasound guided pleural biopsy specimens for pleural tuberculosis. Int. J. Infect. Dis. 108, 89–95 (2021)
    • 67. Li C, Liu C, Sun B et al. Performance of Xpert® MTB/RIF in diagnosing tuberculous pleuritis using thoracoscopic pleural biopsy. BMC Infect. Dis. 20(1), 840 (2020).
    • 68. Du J, Huang Z, Luo Q et al. Rapid diagnosis of pleural tuberculosis by Xpert MTB/RIF assay using pleural biopsy and pleural fluid specimens. J. Res. Med. Sci. 20(1), 26–31 (2015).
    • 69. Gao S, Wang C, Yu X et al. Xpert MTB/RIF Ultra enhanced tuberculous pleurisy diagnosis for patients with unexplained exudative pleural effusion who underwent a pleural biopsy via thoracoscopy: a prospective cohort study. Int. J. Infect. Dis. 106, 370–375 (2021).
    • 70. Lusiba JK, Nakiyingi L, Kirenga BJ et al. Evaluation of Cepheid's Xpert MTB/Rif test on pleural fluid in the diagnosis of pleural tuberculosis in a high prevalence HIV/TB setting. PLOS ONE 9(7), e102702 (2014).
    • 71. WHO meeting report of a technical expert consultation: non-inferiority analysis of Xpert MTB/RIF ultra compared to Xpert MTB/RIF (2017). https://apps.who.int/iris/handle/10665/254792
    • 72. Chakravorty S, Simmons AM, Rowneki M et al. The new Xpert MTB/RIF Ultra: improving detection of Mycobacterium tuberculosis and resistance to rifampin in an assay suitable for point-of-care testing. mBio 8(4), e00812-17 (2017). • This article investigated the analytical performance of the GeneXpert-MTB/RIF Ultra.
    • 73. Bisognin F, Lombardi G, Lombardo D, Re MC, Dal Monte P. Improvement of Mycobacterium tuberculosis detection by Xpert MTB/RIF Ultra: a head-to-head comparison on Xpert-negative samples. PLoS One 13(8), e0201934 (2018).
    • 74. Wang G, Wang S, Yang X et al. Accuracy of Xpert MTB/RIF Ultra for the diagnosis of pleural TB in a multicenter cohort study. Chest 157(2), 268–275 (2020). • This multicenter study compares the diagnostic accuracy of GeneXpert-MTB/RIF Ultra and GeneXpert-MTB/RIF.
    • 75. Meldau R, Randall P, Pooran A et al. Same-day tools, including Xpert Ultra and IRISA-TB, for rapid diagnosis of pleural tuberculosis: a prospective observational study. J. Clin. Microbiol. 57(9), e00614-19 (2019).
    • 76. Rice JE, Reis AH Jr, Rice LM, Carver-Brown RK, Wangh LJ. Fluorescent signatures for variable DNA sequences. Nucleic Acids Res. 40(21), e164 (2012).
    • 77. Eigner U, Veldenzer A, Holfelder M. Evaluation of the FluoroType MTB assay for the rapid and reliable detection of Mycobacterium tuberculosis in respiratory tract specimens. Clin. Lab. 59(9–10), 1179–1181 (2013).
    • 78. Haasis C, Rupp J, Andres S et al. Validation of the FluoroType® MTBDR assay using respiratory and lymph node samples. Tuberculosis (Edinb.) 113, 76–80 (2018).
    • 79. Hofmann-Thiel S, Hoffmann H. Evaluation of Fluorotype MTB for detection of Mycobacterium tuberculosis complex DNA in clinical specimens from a low-incidence country. BMC Infect. Dis. 14, 59 (2014).
    • 80. Obasanya J, Lawson L, Edwards T et al. FluoroType MTB system for the detection of pulmonary tuberculosis. ERJ Open Res. 3(2), 00113-2016 (2017).
    • 81. De Vos M, Derendinger B, Dolby T et al. Diagnostic accuracy and utility of FluoroType MTBDR, a new molecular assay for multidrug-resistant tuberculosis. J. Clin. Microbiol. 56(9), 00113-2016 (2018).
    • 82. Bielsa S, Bernet A, Civit C, Acosta C, Manonelles A, Porcel JM. FluoroType® MTB in pleural fluid for diagnosing tuberculosis. Rev. Clin. Esp. (Barc.) 221(3), 139–144 (2021).
    • 83. Notomi T, Mori Y, Tomita N, Kanda H. Loop-mediated isothermal amplification (LAMP): principle, features, and future prospects. J. Microbiol. 53(1), 1–5 (2015).
    • 84. Nagai K, Horita N, Yamamoto M et al. Diagnostic test accuracy of loop-mediated isothermal amplification assay for Mycobacterium tuberculosis: systematic review and meta-analysis. Sci. Rep. 6, 39090 (2016).
    • 85. Yan L, Xiao H, Zhang Q. Systematic review: comparison of Xpert MTB/RIF, LAMP and SAT methods for the diagnosis of pulmonary tuberculosis. Tuberculosis (Edinb.) 96, 75–86 (2016).
    • 86. Yang B, Wang X, Li H, Li G, Cao Z, Cheng X. Comparison of loop-mediated isothermal amplification and real-time PCR for the diagnosis of tuberculous pleurisy. Lett. Appl. Microbiol. 53(5), 525–531 (2011).
    • 87. Han M, Xiao H, Yan L. Diagnostic performance of nucleic acid tests in tuberculous pleurisy. BMC Infect. Dis. 20(1), 242 (2020).
    • 88. French DJ, Archard CL, Brown T, McDowell DG. HyBeacon probes: a new tool for DNA sequence detection and allele discrimination. Mol. Cell. Probes 15(6), 363–374 (2001).
    • 89. Yan L, Tang S, Yang Y et al. A large cohort study on the clinical value of simultaneous amplification and testing for the diagnosis of pulmonary tuberculosis. Medicine (Baltimore) 95(4), e2597 (2016).
    • 90. Cui Z, Wang Y, Fang L et al. Novel real-time simultaneous amplification and testing method to accurately and rapidly detect Mycobacterium tuberculosis complex. J. Clin. Microbiol. 50(3), 646–650 (2012).
    • 91. Deng S, Sun Y, Xia H et al. Accuracy of commercial molecular diagnostics for the detection of pulmonary tuberculosis in China: a systematic review. Sci. Rep. 9(1), 4553 (2019).
    • 92. Zhang Q, Zhou C. Comparison of laboratory testing methods for the diagnosis of tuberculous pleurisy in China. Sci. Rep. 7(1), 4549 (2017).
    • 93. Nathavitharana RR, Garcia-Basteiro AL, Ruhwald M, Cobelens F, Theron G. Reimagining the status quo: how close are we to rapid sputum-free tuberculosis diagnostics for all? EBioMedicine 78, 103939 (2022).
    • 94. Soni A, Guliani A, Nehra K, Mehta PK. Insight into diagnosis of pleural tuberculosis with special focus on nucleic acid amplification tests. Expert Rev. Respir. Med. 16(8), 887–906 (2022).
    • 95. Yan Z, Wang H, Mu L, Hu ZD, Zheng WQ. Regulatory roles of extracellular vesicles in immune responses against Mycobacterium tuberculosis infection. World J. Clin. Cases 9(25), 7311–7318 (2021).
    • 96. Zhao W, Cao XS, Han YL, Wen XH, Zheng WQ, Hu ZD. Diagnostic utility of pleural cell-free nucleic acids in undiagnosed pleural effusions. Clin. Chem. Lab. Med. 60(10), 1518–1524 (2022).
    • 97. Sorolla MA, Sorolla A, Parisi E, Salud A, Porcel JM. Diving into the pleural fluid: liquid biopsy for metastatic malignant pleural effusions. Cancers (Basel) 13(11), 2798 (2021).
    • 98. Hooper C, Lee YC, Maskell N, BTS Pleural Guideline Group. Investigation of a unilateral pleural effusion in adults: British Thoracic Society Pleural Disease guideline 2010. Thorax 65(Suppl.2), ii4–17 (2010). • This is the British Thoracic Society guideline for pleural effusion management.
    • 99. Liang QL, Shi HZ, Wang K, Qin SM, Qin XJ. Diagnostic accuracy of adenosine deaminase in tuberculous pleurisy: a meta-analysis. Respir. Med. 102(5), 744–754 (2008).
    • 100. Aggarwal AN, Agarwal R, Sehgal IS, Dhooria S. Adenosine deaminase for diagnosis of tuberculous pleural effusion: a systematic review and meta-analysis. PLOS ONE 14(3), e0213728 (2019).
    • 101. Palma RM, Bielsa S, Esquerda A, Martinez-Alonso M, Porcel JM. Diagnostic accuracy of pleural fluid adenosine deaminase for diagnosing tuberculosis. Meta-analysis of Spanish studies. Arch. Bronconeumol. (Engl. Ed.) 55(1), 23–30 (2019).
    • 102. Aggarwal AN, Agarwal R, Sehgal IS, Dhooria S, Behera D. Meta-analysis of Indian studies evaluating adenosine deaminase for diagnosing tuberculous pleural effusion. Int. J. Tuberc. Lung Dis. 20(10), 1386–1391 (2016).