Nucleic acid amplification tests in the diagnosis of tuberculous pleuritis: a systematic review and meta-analysis

BMC Infectious Diseases

John M Colford¹  Lee W Riley³  Alan Hubbard²  Laura L Flores³  Madhukar Pai¹ 

[1] Division of Epidemiology, School of Public Health University of California, Berkeley 140, Warren Hall, Berkeley, CA 94720, USA;Division of Biostatistics, School of Public Health University of California, Berkeley 140, Warren Hall, Berkeley, CA 94720, USA;Division of Infectious Diseases, School of Public Health University of California, Berkeley 140, Warren Hall, Berkeley, CA 94720, USA

关键词: meta-analysis;    accuracy;    polymerase chain reaction;    nucleic acid amplification tests;    tuberculous pleuritis;   

Others  :  1177102
DOI  :  10.1186/1471-2334-4-6

 received in 2003-11-21, accepted in 2004-02-23,  发布年份 2004

【 摘 要 】

Background

Conventional tests for tuberculous pleuritis have several limitations. A variety of new, rapid tests such as nucleic acid amplification tests – including polymerase chain reaction – have been evaluated in recent times. We conducted a systematic review to determine the accuracy of nucleic acid amplification (NAA) tests in the diagnosis of tuberculous pleuritis.

Methods

A systematic review and meta-analysis of 38 English and Spanish articles (with 40 studies), identified via searches of six electronic databases, hand searching of selected journals, and contact with authors, experts, and test manufacturers. Sensitivity, specificity, and other measures of accuracy were pooled using random effects models. Summary receiver operating characteristic curves were used to summarize overall test performance. Heterogeneity in study results was formally explored using subgroup analyses.

Results

Of the 40 studies included, 26 used in-house ("home-brew") tests, and 14 used commercial tests. Commercial tests had a low overall sensitivity (0.62; 95% confidence interval [CI] 0.43, 0.77), and high specificity (0.98; 95% CI 0.96, 0.98). The positive and negative likelihood ratios for commercial tests were 25.4 (95% CI 16.2, 40.0) and 0.40 (95% CI 0.24, 0.67), respectively. All commercial tests had consistently high specificity estimates; the sensitivity estimates, however, were heterogeneous across studies. With the in-house tests, both sensitivity and specificity estimates were significantly heterogeneous. Clinically meaningful summary estimates could not be determined for in-house tests.

Conclusions

Our results suggest that commercial NAA tests may have a potential role in confirming (ruling in) tuberculous pleuritis. However, these tests have low and variable sensitivity and, therefore, may not be useful in excluding (ruling out) the disease. NAA test results, therefore, cannot replace conventional tests; they need to be interpreted in parallel with clinical findings and results of conventional tests. The accuracy of in-house nucleic acid amplification tests is poorly defined because of heterogeneity in study results. The clinical applicability of in-house NAA tests remains unclear.

【 授权许可】

   
2004 Pai et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

【 图 表 】

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【 参考文献 】

• [1]Markowitz N, Hansen NI, Hopewell PC, Glassroth J, Kvale PA, Mangura BT, Wilcosky TC, Wallace JM, Rosen MJ, Reichman LB: Incidence of tuberculosis in the United States among HIV-infected persons. The Pulmonary Complications of HIV Infection Study Group. Ann Intern Med 1997, 126:123-132.
• [2]Centers for Disease Control and Prevention: Reported Tuberculosis in the United States, 2001. [http://www.cdc.gov/nchstp/tb/surv/surv2001/default.htm] webciteAtlanta 2001.
• [3]Rose AMC, Watson JM, Graham C, Nunn AJ, Drobniewski F, Ormerod LP, Darbyshire JH, Leese J: Tuberculosis at the end of the 20th century in England and Wales: results of a national survey in 1998. Thorax 2001, 56:173-179.
• [4]Light RW: Pleural Diseases. Philadelphia: Lippincott Williams & Wilkins; 2001.
• [5]Valdes L, Alvarez D, Valle JM, Pose A, San Jose E: The etiology of pleural effusions in an area with high incidence of tuberculosis. Chest 1996, 109:158-162.
• [6]Liam CK, Lim KH, Wong CM: Causes of pleural exudates in a region with a high incidence of tuberculosis. Respirology 2000, 5:33-38.
• [7]al-Quorain A, Larbi EB, al-Muhanna F, Satti MB, Baloush A, Falha K: Pattern of pleural effusion in Eastern Province of Saudi Arabia: a prospective study. East Afr Med J 1994, 71:246-249.
• [8]Mehta JB, Dutt A, Harvill L, Mathews KM: Epidemiology of extrapulmonary tuberculosis. A comparative analysis with pre-AIDS era. Chest 1991, 99(5):1134-8.
• [9]Frye MD, Pozsik CJ, Sahn SA: Tuberculous pleurisy is more common in AIDS than in non-AIDS patients with tuberculosis. Chest 1997, 112:393-397.
• [10]Bueno EC, Clemente GM, Castro CB, Martin ML, Ramos RS, Panizo GA, Glez-Rio MJ: Cytologic and bacteriologic analysis of fluid and pleural biopsy specimens with Cope's needle. Study of 414 patients. Arch Intern Med 1990, 150:1190-1194.
• [11]Berger HW, Mejia E: Tuberculous pleurisy. Chest 1973, 63:88-92.
• [12]Valdes L, Alvarez D, Jose SE, Penela P, Valle JM, Garcia-Pazos JM, Suarez J, Pose A: Tuberculous pleurisy: a study of 254 patients. Arch Intern Med 1998, 158:2017-2021.
• [13]Seibert AF, Haynes J, Middleton R, Bass JB: Tuberculous pleural effusion: twenty-year experience. Chest 1991, 99:883-886.
• [14]Perez-Rodriguez E, Castro DJ: The use of adenosine deaminase and adenosine deaminase isoenzymes in the diagnosis of tuberculous pleuritis. Curr Opin Pulm Med 2000, 6:259-266.
• [15]American Thoracic Society: American Thoracic Society Workshop. Rapid diagnostic tests for tuberculosis. What is the appropriate use? Am J Respir Crit Care Med 1997, 155:1804-1814.
• [16]Centers for Disease Control and Prevention: Update: Nucleic acid amplification tests for tuberculosis. MMWR Morb Mortal Wkly Rep 2000, 49:593-594.
• [17]Deville WL, Buntinx F, Bouter LM, Montori VM, de Vet HC, van der Windt DA, Bezemer PD: Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2002, 2(1):9. BioMed Central Full Text
• [18]Cochrane Methods Group on Systematic Review of Screening and Diagnostic Tests: Recommended Methods. [http://www.cochrane.org/cochrane/sadtdoc1.htm] webciteCochrane Collaboration 1996.
• [19]Deeks JJ: Systematic reviews in health care: Systematic reviews of evaluations of diagnostic and screening tests. BMJ 2001, 323(7305):157-162.
• [20]Lau J: Meta-Test version 0.6. [http://www.cochrane.org/cochrane/sadt.htm] webciteNew England Medical Center, Boston 1997.
• [21]Littenberg B, Moses LE: Estimating diagnostic accuracy from multiple conflicting reports: a new meta-analytic method. Med Decis Making 1993, 13:313-321.
• [22]Song F, Khan KS, Dinnes J, Sutton AJ: Asymmetric funnel plots and publication bias in meta-analyses of diagnostic accuracy. Int J Epidemiol 2002, 31:88-95.
• [23]Egger M, Smith GD, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315:629-634.
• [24]Abanto SMH, Hirata MH, Hirata RDC, Mamizuka EM, Schmal M, Hoshino-Shimizu S: Evaluation of Henes-PCR assay for Mycobacterium detection in different clinical specimens from patients with or without tuberculosis-associated HIV infection. J Clin Lab Anal 2000, 14:238-245.
• [25]Almeda J, Garcia A, Gonzalez J, Quinto L, Ventura PJ, Vidal R, Rufi G, Martinez JA, Jimenez de Anta MT, Trilla A: Clinical evaluation of an in-house IS6110 polymerase chain reaction for diagnosis of tuberculosis. Eur J Clin Microbiol Infect Dis 2000, 19:859-867.
• [26]Artiles F, Jose Pena M, Isolina Campos-Herrero M, Lafarga B: Clinical evaluation of the Amplified Mycobacterium Tuberculosis Direct 2 test. Enferm Infecc Microbiol Clin 2001, 19:53-56.
• [27]Chan CM, Yuen KY, Chan KS, Yam WC, Yim KH, Ng WF, Ng MH: Single-tube nested PCR in the diagnosis of tuberculosis. J Clin Pathol 1996, 49:290-294.
• [28]D'Amato RF, Hochstein LH, Colaninno PM, Scardamaglia M, Kim K, Mastellone AJ, Patel RC, Alkhuja S, Tevere VJ, Miller A: Application of the Roche Amplicor Mycobacterium tuberculosis (PCR) test to specimens other than respiratory secretions. Diagn Microbiol Infect Dis 1996, 24:15-17.
• [29]Dar L, Sharma SK, Bhanu NV, Broor S, Chakraborty M, Pande JN, Seth P: Diagnosis of pulmonary tuberculosis by polymerase chain reaction for MPB64 gene: an evaluation in a blind study. Indian J Chest Dis Allied Sci 1998, 40:5-16.
• [30]de Lassence A, Lecossier D, Pierre C, Cadranel J, Stern M, Hance AJ: Detection of mycobacterial DNA in pleural fluid from patients with tuberculous pleurisy by means of the polymerase chain reaction: comparison of two protocols. Thorax 1992, 47:265-269.
• [31]de Wit D, Maartens G, Steyn L: A comparative study of the polymerase chain reaction and conventional procedures for the diagnosis of tuberculous pleural effusion. Tuber Lung Dis 1992, 73:262-267.
• [32]de Wit D, Steyn L, Shoemaker S, Sogin M: Direct detection of Mycobacterium tuberculosis in clinical specimens by DNA amplification. J Clin Microbiol 1990, 28:2437-2441.
• [33]Ehlers S, Ignatius R, Regnath T, Hahn H: Diagnosis of extrapulmonary tuberculosis by Gen-Probe amplified Mycobacterium tuberculosis direct test. J Clin Microbiol 1996, 34:2275-2279.
• [34]Gamboa F, Manterola JM, Lonca J, Vinado B, Matas L, Gimenez M, Manzano JR, Rodrigo C, Cardona PJ, Padilla E: Rapid detection of Mycobacterium tuberculosis in respiratory specimens, blood and other non-respiratory specimens by amplification of rRNA. Int J Tuberc Lung Dis 1997, 1:542-555.
• [35]Gamboa F, Manterola JM, Vinado B, Matas L, Gimenez M, Lonca J, Manzano JR, Rodrigo C, Cardona PJ, Padilla E: Direct detection of Mycobacterium tuberculosis complex in nonrespiratory specimens by Gen-Probe Amplified Mycobacterium Tuberculosis Direct Test. J Clin Microbiol 1997, 35:307-310.
• [36]Gunisha P, Madhavan HN, Jayanthi U, Therese KL: Polymerase chain reaction using IS6110 primer to detect Mycobacterium tuberculosis in clinical samples. Indian J Pathol Microbiol 2001, 44:97-102.
• [37]Gracia HMC, Lana AT, Fernandez ML, Fernandez CO, Hernandez JB, Hernandez CC, Macario CC, Lopez AS: Usefulness of a gene amplification technique (LCx MTB) in the diagnosis of tuberculosis: preliminary results with different sputum samples. Arch Bronconeumol 1999, 35:79-83.
• [38]Kaltwasser G, Garcia S, Salinas AM, Montiel F: Enzymatic DNA amplification (PCR) in the diagnosis of extrapulmonary Mycobacterium tuberculosis infection. Mol Cell Probes 1993, 7:465-470.
• [39]Laniado-Laborin R, Enriquez-Rosales ML, Licea Navarroll AF: Diagnosis of tuberculosis by detection of Mycobacterium tuberculosis with a noncommercial polymerase chain reaction. Revista del Instituto Nacional de Enfermedades Respiratorias 2001, 14:22-26.
• [40]Mangiapan G, Vokurka M, Schouls L, Cadranel J, Lecossier D, van Embden J, Hance AJ: Sequence capture-PCR improves detection of mycobacterial DNA in clinical specimens. J Clin Microbiol 1996, 34:1209-1215.
• [41]Martins LC, Paschoal IA, Von Nowakonski A, Silva SA, Costa FF, Ward LS: Nested-PCR using MPB64 fragment improves the diagnosis of pleural and meningeal tuberculosis. Rev Soc Bras Med Trop 2000, 33:253-257.
• [42]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 2000, 4:871-876.
• [43]Miyazaki Y, Koga H, Kohno S, Kaku M: Nested polymerase chain reaction for detection of Mycobacterium tuberculosis in clinical samples. J Clin Microbiol 1993, 31:2228-2232.
• [44]Morcillo NS, Chirico MC, Trovero AC, Vignoles M, Dolmann AL: Clinical utility of a ligase chain reaction commercial kit for the diagnosis of pulmonary and extrapulmonary tuberculosis. Rev Argent Microbiol 2001, 33:187-196.
• [45]Nagesh BS, Sehgal S, Jindal SK, Arora SK: Evaluation of polymerase chain reaction for detection of Mycobacterium tuberculosis in pleural fluid. Chest 2001, 119:1737-1741.
• [46]Palacios JJ, Ferro J, Ruiz Palma N, Roces SG, Villar H, Rodriguez J, Prendes P: Comparison of the ligase chain reaction with solid and liquid culture media for routine detection of Mycobacterium tuberculosis in nonrespiratory specimens. Eur J Clin Microbiol Infect Dis 1998, 17:767-772.
• [47]Pao CC, Yen TS, You JB, Maa JS, Fiss EH, Chang CH: Detection and identification of Mycobacterium tuberculosis by DNA amplification. J Clin Microbiol 1990, 28:1877-1880.
• [48]Parandaman V, Narayanan S, Narayanan PR: Utility of polymerase chain reaction using two probes for rapid diagnosis of tubercular pleuritis in comparison to conventional methods. Indian J Med Res 2000, 112:47-51.
• [49]Pfyffer GE, Kissling P, Jahn EM, Welscher HM, Salfinger M, Weber R: Diagnostic performance of amplified Mycobacterium tuberculosis direct test with cerebrospinal fluid, other nonrespiratory, and respiratory specimens. J Clin Microbiol 1996, 34:834-841.
• [50]Portillo-Gomez L, Morris SL, Panduro A: Rapid and efficient detection of extra-pulmonary Mycobacterium tuberculosis by PCR analysis. Int J Tuberc Lung Dis 2000, 4:361-370.
• [51]Querol JM, Minguez J, Garcia-Sanchez E, Farga MA, Gimeno C, Garcia-de-Lomas J: Rapid diagnosis of pleural tuberculosis by polymerase chain reaction. Am J Respir Crit Care Med 1995, 152:1977-1981.
• [52]Rantakokko-Jalava K, Marjamaki M, Marttila H, Makela 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 2001, 33:55-62.
• [53]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 2000, 31:509-514.
• [54]Reischl U, Lehn N, Wolf H, Naumann L: Clinical evaluation of the automated COBAS AMPLICOR MTB assay for testing respiratory and nonrespiratory specimens. J Clin Microbiol 1998, 36:2853-2860.
• [55]Shah S, Miller A, Mastellone A, Kim K, Colaninno P, Hochstein L, D'Amato R: Rapid diagnosis of tuberculosis in various biopsy and body fluid specimens by the AMPLICOR Mycobacterium tuberculosis polymerase chain reaction test. Chest 1998, 113:1190-1194.
• [56]Tan MF, Ng WC, Chan SH, Tan WC: Comparative usefulness of PCR in the detection of Mycobacterium tuberculosis in different clinical specimens. J Med Microbiol 1997, 46:164-169.
• [57]Tan JAMA, Lee BW, Lim TK, Chin NK, Tan CB, Xia JR, Yap HK, Kumarasinghe G: Detection of Mycobacterium tuberculosis in sputum, pleural and bronchoalveolar lavage fluid using DNA amplification of the MPB 64 protein coding gene and IS6110 insertion element. Southeast Asian J Trop Med Public Health 1995, 26:247-252.
• [58]Verma A, Dasgupta N, Aggrawal AN, Pande JN, Tyagi JS: Utility of a Mycobacterium-Tuberculosis GC-rich repetitive sequence in the diagnosis of tuberculous pleural effusion by PCR. Indian J Biochem Biophys 1995, 32:429-436.
• [59]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 2000, 118:1355-1364.
• [60]Villena V, Rebollo MJ, Aguado JM, Galan A, Lopez Encuentra A, Palenque E: Polymerase chain reaction for the diagnosis of pleural tuberculosis in immunocompromised and immunocompetent patients. Clin Infect Dis 1998, 26:212-214.
• [61]Vlaspolder F, Singer P, Roggeveen C: Diagnostic value of an amplification method (Gen-Probe) compared with that of culture for diagnosis of tuberculosis. J Clin Microbiol 1995, 33:2699-2703.
• [62]Valdes L, Jose SE, Alvarez D, Sarandeses A, Pose A, Chomon B, Alvarez-Dobano JM, Salgueiro M, Suarez JR: Diagnosis of tuberculous pleurisy using the biologic parameters adenosine deaminase, lysozyme, and interferon gamma. Chest 1993, 103:458-465.
• [63]Aoe K, Hiraki A, Murakami T, Eda R, Maeda T, Sugi K, Takeyama H: Diagnostic significance of Interferon-γ in tuberculous pleural effusions. Chest 2003, 123:740-744.
• [64]Greco S, Girardi E, Masciangelo R, Capoccetta GB, Saltini C: Adenosine deaminase and interferon gamma measurements for the diagnosis of tuberculous pleurisy: a meta-analysis. Int J Tuberc Lung Dis 2003, 7:777-86.
• [65]Woods GL: Molecular techniques in mycobacterial detection. Arch Pathol Lab Med 2001, 125:122-126.
• [66]Noordhoek GT, van Embden JDA, Kolk AHJ: Reliability of nucleic acid amplification for detection of Mycobacterium tuberculosis : an international collaborative quality control study among 30 laboratories. J Clin Microbiol 1996, 34:2522-2525.
• [67]Knottnerus JA, van Weel C, Muris JW: Evaluation of diagnostic procedures. BMJ 2002, 324:477-80.
• [68]Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, Bossuyt PM: Empirical evidence of design-related bias in studies of diagnostic tests. JAMA 1999, 282:1061-1066.
• [69]van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, Gicquel B, Hermans P, Martin C, McAdam R, Shinnick TM: Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol 1993, 31:406-409.
• [70]Sarmiento OL, Weigle KA, Alexander J, Weber DJ, Miller WC: Assessment by meta-analysis of PCR for diagnosis of smear-negative pulmonary tuberculosis. J Clin Microbiol 2003, 41(7):3233-40.
• [71]Pai M, Flores LL, Pai N, Hubbard A, Riley LW, Colford JM Jr: Diagnostic accuracy of nucleic acid amplification tests for tuberculous meningitis: a systematic review and meta-analysis. Lancet Infect Dis 2003, 3:633-43.