Comparison of the Xpert MTB/RIF Assay and Real-time PCR for the Detection of Mycobacterium tuberculosis
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1 Available online at Annals of Clinical & Laboratory Science, vol. 45, no. 3, Comparison of the Xpert MTB/RIF Assay and Real-time PCR for the Detection of Mycobacterium tuberculosis Min Jin Kim 1,2, You Sun Nam 3, Sun Young Cho 4, Tae Sung Park 4, and Hee Joo Lee 4 1 Department of Laboratory Medicine, Graduate School of Medicine, Kyung Hee University, 2 Seegene Medical Foundation, 3 Department of Biomedical Science, Graduate School, Kyung Hee University, and 4 Department of Laboratory Medicine, School of Medicine, Kyung Hee University, Seoul, Republic of Korea Abstract. Introduction. We compared the Xpert MTB/RIF assay with a real-time PCR assay using samples from culture-positive patients with TB. In addition, drug susceptibility test results were compared to evaluate the usefulness of these methods. Materials and Methods. Fifty-two clinical specimens were analyzed by standard smear-microscopy, mycobacterial growth indicator tube (MGIT) culture, solid culture, MGIT drug-susceptibility testing, TB real-time PCR, and the Xpert MTB/RIF assay. Results. Diagnostic sensitivity of AdvanSure TB/NTM real-time PCR was 80.0%. As shown from smear positive and negative specimens, sensitivities were 87.5% and 75.9%, respectively. The diagnostic sensitivity of Xpert MTB/RIF assay was 75.5%, and from smear positive and negative specimens, sensitivities were 93.8% and 65.5%, respectively. There were 10 cases with discrepant results between two methods. 2 cases were found resistant to rifampin, although Xpert MTB/RIF assay was able to detect rifampin resistance in only one specimen. Discussion. Xpert MTB/RIF assay is an easier method to conduct and while its ability to detect rifampin resistance simultaneously is a benefit, its sensitivity from smear negative-culture positive specimens was lower than Advansure TB/NTM real-time PCR. Further investigation to increase the sensitivity and detect other drug resistances by kit-based assays is required for the rapid and accurate diagnosis of tuberculosis. Keywords: Mycobacterium tuberculosis, Xpert, Real-Time Polymerase Chain Reaction, Smear-negative Introduction Tuberculosis (TB) is one of the serious infectious diseases along with malaria and human immunodeficiency virus (HIV) infection, globally. According to the World Health Organization report in 2010, 880 million TB patients occurred globally and resulted in 1.1 million deaths [1]. In South Korea, the registry number of new tuberculosis patients was 36,305, and 2,365 died of tuberculosis in 2010 [2]. Due to the lack of effective prevention so far, it is important to diagnose and treat TB in its early stage to minimize additional infection. When TB is suspected, chest X-ray, sputum smear, and culture assay are conducted. For the culture method, cultivation takes up to 8 weeks at most and therefore suffers from slow diagnosis. Recently, however, molecular biological methods such as polymerase chain reaction (PCR), which Address correspondence to Hee Joo Lee, MD., PhD., Department of Laboratory Medicine, School of Medicine, Kyung Hee University, 1 Hoegi-dong, Dongdaemun-gu, Seoul , Korea; phone: ; fax: ; e mail: leehejo@khmc.or.kr amplifies specific DNA existing in the tubercular bacillus for identification, have developed. Although PCR cannot fully replace acid fast bacilli (AFB) smear and culture methods, it offers high specificity, shorter duration, and higher sensitivity than AFB smear and culture methods so it is considered as a useful complementary test for TB diagnosis [3,4]. Since such molecular biological methods can assist TB diagnosis on smear negative TB patients, time to treatment can be shortened. The development of a rapid molecular test that can simultaneously conduct TB diagnosis and drug susceptibility test has also enabled effective selection of treatment drugs. In this study, recently developed Xpert MTB/RIF assay (Cepheid Inc., Sunnyvale, CA, USA) and TB real-time PCR are compared by dividing patients who showed positive results in culture assay, considered as the gold standard for TB diagnosis, into smear positive and negative patients. Also, drug susceptibility is compared in order to see whether such tests contribute to TB diagnosis /15/ by the Association of Clinical Scientists, Inc.
2 328 Annals of Clinical & Laboratory Science, vol. 45, no. 3, 2015 Materials and Methods Subjects. This study was conducted at Kyung Hee Medical Center, Seoul, South Korea from October 2011 to June 2012, on 52 specimens that requested TB test. These 52 clinical specimens were isolated from 50 patients, 45 of whom were diagnosed as Mycobacterium tuberculosis (MTB). Among them, there were 16 smear positive-culture positive specimens with 1 rifampin-resistant and 29 smear negative-culture positive specimens with 1 rifampin-resistant. There were 7 specimens that were not diagnosed as MTB, where 2 of them, sputum and bronchial washing, were collected from a patient diagnosed as TB 9 months ago and was currently under drug treatment, and the other 5 specimens were from non-tb respiratory patients (4 pneumonia, 1 Chronic obstructive pulmonary disease (COPD)) consisting of 4 sputum and 1 bronchial washing. The clinical specimens included respiratory and nonrespiratory specimens, and they were stored at -70 C (Table 1). Respiratory specimen included 36 sputum samples and 10 bronchial washing samples. Nonrespiratory specimen included 3 pleural fluid samples, 1 pleural mass, and 2 urine samples. Ethical approval was waived for this study in South Korea, since it did not involve human subject or human data, but only the isolated microorganisms from remnant specimen of analytical process. We declare that the result of this study was not used for patient care or any other purposes. Sample processing. The direct smears were scored according to WHO/IUATLD guidelines as AFB by fluorescence microscopy negative, 1+, 2+, or 3+ [5]. After decontamination with 2% sodium hydroxide N-acetyl- L-cysteine sodium hydroxide (Becton Dickinson, Sparks, MD, USA) and centrifugation at 3000 g for 20 min, the sediments of specimens are neutralized with sterile phosphate-buffered saline (PBS; ph 6.8) and inoculated solid culture using 3% ogawa medium and liquid culture using BACTEC MGIT 960 system (Becton Dickinson, Sparks, MD, USA). Automated Bactec MGIT 960 system was used according to the manufacturer s instructions [6]. Real-time PCR. TB real-time PCR was conducted with AdvanSure TB/NTM real-time PCR kit (LG Lifescience, Seoul, Korea) with the SLAN real-time PCR detection system (LG Lifescience), looking for primer reactions on specific genes in the MTB complex, IS6110, and mycobacteria ITS. During the process, DNA was extracted from the patient s specimen, which was added into PCR tubes with PCR mixtures along with positive and negative controls and primer/probe mix. After centrifugation, reaction was conducted by adding the mixture into the real-time PCR cycler. As for PCR conditions, 1 cycle was conducted at 50 C, 2 minutes, 1 cycle at 95 C, 10 minutes, 30 cycles of 10 s at 95 C and 40 s at 62 C to confirm the threshold cycle and reaction results [7]. Xpert MTB/RIF assay (Cepheid Inc., Sunnyvale, CA, USA) was accomplished by way of the following: 1 ml of the resuspended sample was mixed with 2 ml Xpert sample reagent, shaken several times, and incubated for 15 min at room temperature as per manufacturer instruction. This mixture was transferred into an Xpert cartridge and inserted into the GeneXpert instrument. Cycle thresholds (C Ts ) of 5 rpob gene probes automatically reported the presence of M. tuberculosis (GeneXpert Dx software, version 2.1) [8]. Xpert MTB/RIF assay semi-quantitatively estimates the concentration of bacilli as defined by the CT range [9]. Rifampin resistance was reported automatically by calculation of a change in C T (ΔC T ) between the highest and the lowest signal of the 5 probes. For rifampin resistant mutants, Rif resistance detected is reported when ΔC T is greater or equal to 3.5. Anti-TB drug susceptibility testing (DST). Culturebased drug susceptibility testing (DST) was examined by agar proportion method performed with Middlebrook 7H10 agar and absolute concentration method with Lowenstein Jensen medium according to the CLSI guideline M24-A2 [10]. 15 antibiotics (Isoniazid(INH), Rifampin(RFP), Pyrazinamide(PZA), Ethambutol(EMB) Streptomycin, Cycloserine(CS), Ethionamide, Prothionamide(PTH), Para amino salicylic acid(pas), ofloxacin, rifabutin, Fluoroquinolone, Amikacin, Kanamycin, Capreomycin) went through DST. Results Comparison of the results between the Xpert MTB/RIF assay and the real-time PCR. AdvanSure TB/NTM real-time PCR and Xpert MTB/RIF assay were conducted on 45 TB diagnosed specimens and 7 non-tb diagnosed specimens. The diagnostic sensitivity of AdvanSure TB/ NTM real-time PCR was 80.0%, showing 87.5% sensitivity for smear positive specimen and 75.9% for smear negative specimen. The specificity was 85.7% (Table 2). For Xpert MTB/RIF assay, diagnostic sensitivity was 75.5%, showing 93.8% sensitivity on smear positive and 65.5% sensitivity on smear negative specimen. Its specificity was 85.7%. Discrepancy of results between the Xpert MTB/ RIF assay and the real-time PCR. There was a case 1 where smear positive specimens showed negative results in Advansure TB/NTM real-time PCR while urine specimen in Xpert MTB/RIF assay
3 The detection of Mycobacterium tuberculosis 329 Table 1. The composition of clinical specimens. Tuberculosis patients Non tuberculosis patients Specimen Smear-positive Smear-negative Smear-negative (total no.) culture-positive culture-positive culture- negative specimens (16) specimens (29) specimens (7) Sputum Bronchial washing Pleural fluid Pleural mass Urine Table 2. Clinical sensitivity and specificity of Advansure TB/NTM real-time PCR and the Xpert MTB/RIF assay using culture as the gold standard. Test Advansure TB/NTM real-time PCR Xpert MTB/RIF assay (no.of specimens positive/no.of (no.of specimens positive/no.of specimens positive by culture) specimens positive by culture) Sensitivity, all 80.0% (36/45) 75.5% (34/45) Sensitivity, smear positive 87.5% (14/16) 93.8% (15/16) Sensitivity, smear negative 75.9% (22/29) 65.5% (19/29) Specificity 85.7% (6/7) 85.7% (6/7) showed low detection (Table 3). For smear negative specimens in Table 3, 6 specimens showed positive results only in Advansure TB/NTM real-time PCR (case 2-7). Among smear negative specimens, 3 showed negative results in Advansure TB/NTM real-time PCR. Solid culture results for 3 specimens were reported as 2+ (case 8-10). There was a sputum specimen that showed false positive results in the two PCR methods (case 11). This specimen was collected from a patient who was diagnosed as TB 9 months ago and was currently under medication. Comparison of antituberculosis drug susceptibility testing results. For specimens diagnosed as TB, 16 specimens showed smear positive results, of which one sputum specimen showed isoniazid, rifampin, and ethanbutol resistance. For this specimen, Xpert MTB/RIF assay also showed rifampin resistance. Among 29 smear negative TB specimens, streptomycin, rifampin, and rifabutin resistance were observed in one bronchial washing, but PCR results in Xpert MTB/RIF assay showed no detection and could not confirm rifampin resistance (Table 4). Discussion Xpert is an automated molecular test in which its plastic cartridge includes all necessary reaction solvents for cell lysis, DNA extraction, amplification, and detection. It automatically initiates PCR when the preconditioned sputum is inserted to the MTB/ RIF cartridge and into the GeneXpert machine, showing results for tubercular bacillus and rifampin resistance within 2 hours. However, this test is costly and it cannot confirm isoniazid resistance. Nonetheless, the WHO recommended its active use for MDR TB control in 2011 [11]. When the results between Advansure TB/NTM real-time PCR and Xpert MTB/RIF assay on specimens from TB patients were compared (Table 2), the overall sensitivity for Advansure TB/NTM realtime PCR was 80.0%, which was higher than Xpert MTB/RIF assay at 75.5%. For Smear positive specimens, Xpert MTB/RIF assay showed 93.8% sensitivity, which was higher than Advansure TB/NTM real-time PCR at 87.5%. On the other hand, for smear negative specimens, Xpert MTB/
4 330 Annals of Clinical & Laboratory Science, vol. 45, no. 3, 2015 Table 3. Discrepant results of Advansure TB/NTM real-time PCR and Xpert MTB/RIF assay. Case Specimen AFB smear Liquid Solid Advansure Xpert MTB/RIF culture culture TB/NTM real-time PCR* assay 1 Urine 1+ MTB 1+ Negative Low detected 2 Bronchial washing Negative MTB 1+ Positive Not detected 3 Sputum Negative MTB 1+ Positive Not detected 4 Pleural fluid Negative MTB 1+ Positive Not detected 5 Pleural fluid Negative NT 1+ Positive Not detected 6 Sputum Negative No growth 1+ Positive Not detected 7 Bronchial washing Negative MTB 1+ Positive Not detected 8 Sputum Negative MTB 2+ Negative Very low detected 9 Urine Negative MTB 2+ Negative Low detected 10 Sputum Negative MTB 2+ Negative Very low detected 11 Sputum Negative No growth No growth Positive Very low detected Abbreviation: AFB, acid fast bacilli; MTB, Mycobacterium tuberculosis. *For MTB, cycle threshold (Ct) less than 35 was determined as positive in Advansure TB/NTM real-time PCR. Xpert MTB/RIF assay semi-quantitatively estimates the concentration of bacilli as defined by the CT range (high, <16; medium, 16 22; low, 22 28; very low, >28) Table 4. Comparison of specimens exhibiting rifampicin resistance. No. Specimen AFB smear Liquid Solid Xpert rifampin Elapsed Resistant culture culture MTB/RIF resistance time drug assay* from requisition of specimen to DST result. 1 Sputum 2+ MTB 1+ Medium detected 80 days Rifampin, Isonizid Ethanbutol 2 Bronchial Negative MTB 1+ Not detect Not detected 96 days Rifampin, washing Streptomycin Rifabutin Abbreviation: AFB, acid fast bacilli; MTB, mycoplasma tuberculosis *Xpert MTB/RIF assay semi-quantitatively estimates the concentration of bacilli as defined by the C T range (high, <16; medium, 16 22; low, 22 28; very low, >28) RIF assay showed 65.5% sensitivity, which was lower than Advansure TB/NTM real-time PCR at 75.9%. The low sensitivity of two PCR assays among smear negative specimen appears to be affected by the inclusion of nonrespiratory specimens, which supposedly have lower number of TB particles compared to those from smear positive specimens. Previously, Miller et al. compared Xpert MTB/RIF assay and IS6110 real-time PCR outcomes with TB specimens, and found that the sensitivity of Xpert MTB/RIF assay was 92%, which was higher than real-time PCR at 81% [12]. When the specimens were divided into smear positive/negative and pulmonary/extrapulmonary specimens, Xpert MTB/ RIF assay showed higher sensitivity than real-time PCR. According to Armand et al., Xpert MTB/RIF assay was compared to IS6110-TaqMan real-time PCR with clinical specimens that were culture positive for Mycobacterium tuberculosis. This comparison found that Xpert MTB/RIF assay showed excellent sensitivity (100%) with smear-positive specimens while smear-negative specimens yielded 48% sensitivity in Xpert MTB/RIF assay, which was lower than IS6110-TaqMan real-time PCR at 69% [13]. This
5 study showed similar results to the latter study where Xpert MTB/RIF assay showed low sensitivity. Given that the two previous studies with similar sample size of 100 specimens showed different findings in sensitivity and the fact that there are no large scale studies on real-time PCR performance, future investigation should include cooperative research on Xpert MTB/RIF assay and real-time PCR. There were 11 cases that showed discrepancy between two test results (Table 3). For case 1, the same specimen turned out to be positive by showing 1+ in solid culture and therefore its Advansure TB/NTM real-time PCR results were considered as false negatives. From case 2 to 7, the Ct of the Advansure TB/NTM real-time PCR ranged from to Considering the manufacturer s instruction where the Ct value up to 35 is considered as positive, it seemed that Xpert MTB/RIF assay showed false negative results due to the difference in limit of detection (LOD) stemming from fewer bacteria. From case 8 to 10, only Xpert MTB/RIF assay showed positive results while culture showed 2+ and Advansure TB/NTM real-time PCR showed false negatives. For case 11, two PCR tests showed positive results for a culture negative PCR positive specimen. This specimen was collected from a patient diagnosed as TB 9 months ago and was currently under medication, and therefore the PCR positive result seems to be related to amplification of DNA that were released from dead cells [14]. Out of 11 cases that showed discordant results, 4 were extrapulmonary specimens. Considering that the manufacturer recommends respiratory specimen for Xpert MTB/RIF assay and the limited number of cases showing discordant results on nonrespiratory specimen included in this study, its usage on non-respiratory specimen requires more careful consideration and future large-scale validation. For 2 specimens that showed rifampin resistance, Xpert MTB/RIF assay detected rifampin resistance for one but it could not detect the other (Table 4). The bronchial washing specimen, in which rifampin resistance was not detected, showed PCR Ct value of in Advansure TB/NTM real-time PCR, resulting in a negative result from the Xpert MTB/RIF assay. Nonetheless, considering the fact The detection of Mycobacterium tuberculosis 331 that it takes 80 days from cultivation to positive findings to drug susceptibility test in conventional practice, Xpert MTB/RIF assay can offer diagnosis as well as rifampin resistance detection and contribute to a swift secondary drug approach. It is, however, acknowledged that certain reports find that false positive rifampin resistance can be detected due to rpob gene mutation or the wild type rpob gene sequence [15,16]. Therefore, careful diagnosis will be required through confirmatory phenotypic or genotypic drug susceptibility testing so that MDR-TB cases are not overdiagnosed, along with a development of compensatory MTB/RIF assays. As for the limits to this study, the fact that it could only work with 57 specimens resulted in a small sample size, where specificity had to be explained with only 7 non-tb patients. Although this study included 6 non-respiratory specimens, its small number could have rendered difficulties in explaining the different results between respiratory and non-respiratory specimen. Also, Xpert MTB/RIF assay could not be conducted on all specimens requested for TB tests and instead applied to specimens showing rifampin resistance and AFB smear negative-culture positive specimens. This is likely to have caused selection bias. Finally, Xpert MTB/RIF assay was conducted on AFB smear negative-culture positive specimens that were kept frozen. Compared to the Advansure TB/NTM real-time PCR that were conducted in proximity with the specimen collection, relatively fresh condition samples were used in the Xpert MTB/RIF assay. The Xpert MTB/RIF assay could not be conducted on the same date as the Advansure TB/NTM real-time PCR, and had to be done with thawed specimens in which tubercular bacillus DNA could have been damaged throughout the freezing and thawing process. This may also affect the Xpert MTB/RIF assay results. PCR test is an important test for TB patients in order to deliver quick diagnosis and treatment. When Advansure TB/NTM real-time PCR and Xpert MTB/RIF assay is compared, Xpert MTB/ RIF assay is useful for its convenience in the test method and simultaneous detection of rifampin resistance. But for AFB smear negative-culture positive specimens, its sensitivity is lower than
6 332 Annals of Clinical & Laboratory Science, vol. 45, no. 3, 2015 Advansure TB/NTM real-time PCR. Therefore, further investigation should seek to develop a kit with increased sensitivity and simultaneous drug susceptibility tests for more drugs other than rifampin so that it can contribute to faster treatment of TB patients. Acknowledgment This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (NRF-2014R1A1A ). The authors thank for Cepheid Inc. (USA) for a donation of Xpert reagents and cartridges. References 1. World Health Organization. Global Tuberculosis Control: WHO Report. Geneva: World Health Organization, Kim HJ. Current Status of Tuberculosis in Korea. Korean J Med. 2012;82(3): Long R. Canadian Tuberculosis Standards. 6th ed. Ottawa: Canadian Lung Association and Public Health Agency of Canada, Diagnostic Standards and Classification of Tuberculosis in Adults and Children. This official statement of the American Thoracic Society and the Centers for Disease Control and Prevention was adopted by the ATS Board of Directors, July This statement was endorsed by the Council of the Infectious Disease Society of America, September Am J Respir Crit Care Med 2000;161: International Union against Tuberculosis and Lung Disease Technical guide: sputum examination for tuberculosis by direct microscopy in low income countries, 5th ed. International Union against Tuberculosis and Lung Disease, Paris, France. 6. Hanna BA, Ebrahimzadeh A, Elliott LB, Morgan MA, Novak SM, Rusch-Gerdes S, et al. Multicenter Evaluation of the BACTEC MGIT 960 System for Recovery of Mycobacteria. J Clin Microbiol 1999;37: Cho SY, Kim MJ, Suh JT, Lee HJ. Comparison of Diagnostic Performance of Three Real-Time PCR Kits for Detecting Mycobacterium Species. Yonsei Med J 2011;52(2): Friedrich SO, Venter A, Kayigire XA, Dawson R, Donald PR, Diacon AH. Suitability of Xpert MTB/RIF and Genotype MTBDRplus for Patient Selection for a Tuberculosis Clinical Trial. J Clin Microbiol 2011;49(8): Lawn SD, Nicol MP. Xpert MTB/RIF assay: development, evaluation and implementation of a new rapid molecular diagnostic for tuberculosis and rifampicin resistance. Future Microbiol. 2011;6(9): National Committee for Clinical Laboratory Standards. Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes: approved standard-second edition. CLSI document M24-A2. Wayne, PA: Clinical and Laboratory Standards Institute, World Health Organization. Tuberculosis Diagnostics Automated DNA Test 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 2011;49: Armand S, Vanhuls P, Delcroix G, Courcol R, Lemaître N. Comparison of the Xpert MTB/RIF Test with an IS6110- TaqMan Real-Time PCR Assay for Direct Detection of Mycobacterium tuberculosis in Respiratory and Nonrespiratory Specimens. J Clin Microbiol 2011;49: Nogva HK, Dromtorp SM, Nissen H, Rudi K. Ethidium Monoazide for DNA-based Differentiation of Viable and Dead Bacteria by 5 -Nuclease PCR. Biotechniques 2003;34:804-8, 810, Williamson DA, Basu I, Bower J, Freeman JT, Henderson G, Roberts SA. An Evaluation of the Xpert MTB/RIF Assay and Detection of False-Positive Rifampicin Resistance in Mycobacterium tuberculosis. Diagn Microbiol Infect Dis 2012;74: Van Rie A, Mellet K, John MA, Scott L, Page-Shipp L, Dansey H, et al. False-Positive Rifampicin Resistance on Xpert MTB/ RIF: Case Report and Clinical Implications. Int J Tuberc Lung Dis 2012;16:
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